Integrated pest management for tropical crops: soyabeans · pest/pathogen,planttissue...

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Integrated pest management for tropical crops: soyabeans E.A. Heinrichs 1 * and Rangaswamy Muniappan 2 Address: 1 IPM Innovation Lab, 6517 S. 19th St., Lincoln, NE, USA. 2 IPM Innovation Lab, CIRED, Virginia Tech, 526 Prices Fork Road, Blacksburg, VA, USA. *Correspondence: E.A. Heinrichs. Email: [email protected] Received: 29 January 2018 Accepted: 16 October 2018 doi: 10.1079/PAVSNNR201813055 The electronic version of this article isthe definitive one. It is located here: http://www.cabi.org/cabreviews © CAB International 2018 (Online ISSN 1749-8848) Abstract Soyabean, because of its importance in food security and wide diversity of uses in industrial applications, is one of the worlds most important crops. There are a number of abiotic and biotic constraints that that threaten soyabean production. Soyabean pests are major biotic constraints limiting soyabean production and quality. Crop losses to animal pests, diseases and weeds in soyabeans average 2629% globally. This review discusses biology, global distribution and plant damage and yield losses in soyabean caused by insect pests, plant diseases, nematodes and weeds. The interactions among insects, weeds and diseases are detailed. A soyabean integrated pest management (IPM) package of practices, covering the crop from pre-sowing to harvest, is outlined. The effect of climate changes on arthropod pests, plant diseases and weeds are discussed. The history and evolution of the highly successful soyabean IPM programme in Brazil and the factors that led to its demise are explained. Keywords: Biological control, Biotic constraints, Chemical control, Climate change, Cultural control, Insect pests, Mechanical practices, Nematodes, Pesticides, Package of practices, Plant diseases, Plant pest interactions, Soybean IPM programme, Weeds Review Methodology: Search terms used were: scientific and common names of all of the insects, plant diseases, nematodes and weeds listed in the tables. Additional search terms were soyabean IPM, management of soyabeanpests, climate change and soyabean pests. The following databases were searched for relevant articles: Agricola and CAB Abstracts from 1960 on, Plantwise, CABI Invasives, Google Scholar, Google Search, Yahoo Search, EPPO Global Database, Encyclopedia of Life, BugGuide, Wikipedia and Center for Invasive Species Research. This was supplemented through personal contacts. Introduction Soyabean, one of the oldest food plants, was domesticated in northeastern China by 1100 BC. Over the next several hundred years the domesticated soyabean (Glycine max) spread throughout much of eastern Asia. It grew upright and yielded larger, more digestible seeds. A variety of foods was developed from the soyabean, ranging from soyabean sprouts to steamed raw beans to roasted seeds to soy milk to soy sauce to fermented soyabean paste and cake to soy flour to the commonly eaten curd called tofu (or doufu) [1]. Soyabeans reached the western world by the early 1700s and were first grown in North America by 1804. Benjamin Franklin appears to have been involved in introducing soyabeans from France to Philadelphia at that time. A number of varieties were grown and evaluated in the United States. Today, the soyabean crop is one of the most important crops worldwide [2]. American soyabean production has been used by the food processing industry in such foods as margarine, shortening, ice cream, salad dressings and mayonnaise. Industry uses smaller amounts in products including paint, ink, putty, caulking, wallpaper, rubber substitutes, adhesives, fire extinguisher foam, electrical insulation and gasoline (ethanol). The versatile soyabean is a part of everyones life in developed countries [1]. The crop is grown on about 6% of the worlds arable land and since the 1970s; the area in soyabean production has the highest increase compared with any other crop [2]. Global soyabean production was 17 million metric tonnes (MMT) in 1960 and increased to 313 MMT in 2015. CAB Reviews 2018 13, No. 055 http://www.cabi.org/cabreviews

Transcript of Integrated pest management for tropical crops: soyabeans · pest/pathogen,planttissue...

Integrated pest management for tropical crops: soyabeans

E.A. Heinrichs1* and Rangaswamy Muniappan2

Address: 1 IPM Innovation Lab, 6517 S. 19th St., Lincoln, NE, USA. 2 IPM Innovation Lab, CIRED, Virginia Tech, 526 Prices Fork Road,Blacksburg, VA, USA.

*Correspondence: E.A. Heinrichs. Email: [email protected]

Received: 29 January 2018Accepted: 16 October 2018

doi: 10.1079/PAVSNNR201813055

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2018 (Online ISSN 1749-8848)

Abstract

Soyabean, because of its importance in food security and wide diversity of uses in industrialapplications, is one of the world’s most important crops. There are a number of abiotic and bioticconstraints that that threaten soyabean production. Soyabean pests are major biotic constraintslimiting soyabean production and quality. Crop losses to animal pests, diseases and weeds insoyabeans average 26–29% globally. This review discusses biology, global distribution and plantdamage and yield losses in soyabean caused by insect pests, plant diseases, nematodes and weeds.The interactions among insects, weeds and diseases are detailed. A soyabean integrated pestmanagement (IPM) package of practices, covering the crop from pre-sowing to harvest, is outlined.The effect of climate changes on arthropod pests, plant diseases and weeds are discussed. The historyand evolution of the highly successful soyabean IPM programme in Brazil and the factors that led to itsdemise are explained.

Keywords: Biological control, Biotic constraints, Chemical control, Climate change, Cultural control, Insect pests,Mechanical practices, Nematodes, Pesticides, Package of practices, Plant diseases, Plant pest interactions,Soybean IPM programme, Weeds

Review Methodology: Search terms used were: scientific and common names of all of the insects, plant diseases, nematodes andweeds listed in the tables. Additional search terms were soyabean IPM, management of soyabean pests, climate change and soyabeanpests. The following databases were searched for relevant articles: Agricola and CAB Abstracts from 1960 on, Plantwise, CABI Invasives,Google Scholar, Google Search, Yahoo Search, EPPO Global Database, Encyclopedia of Life, BugGuide, Wikipedia and Center forInvasive Species Research. This was supplemented through personal contacts.

Introduction

Soyabean, one of the oldest food plants, was domesticatedin northeastern China by 1100 BC. Over the next severalhundred years the domesticated soyabean (Glycine max)spread throughout much of eastern Asia. It grew uprightand yielded larger, more digestible seeds. A variety of foodswas developed from the soyabean, ranging from soyabeansprouts to steamed raw beans to roasted seeds to soymilk to soy sauce to fermented soyabean paste and caketo soy flour to the commonly eaten curd called tofu(or doufu) [1].Soyabeans reached the western world by the early 1700s

and were first grown in North America by 1804. BenjaminFranklin appears to have been involved in introducingsoyabeans from France to Philadelphia at that time.

A number of varieties were grown and evaluated in theUnited States.Today, the soyabean crop is one of the most important

crops worldwide [2]. American soyabean production hasbeen used by the food processing industry – in such foodsas margarine, shortening, ice cream, salad dressings andmayonnaise. Industry uses smaller amounts in productsincluding paint, ink, putty, caulking, wallpaper, rubbersubstitutes, adhesives, fire extinguisher foam, electricalinsulation and gasoline (ethanol). The versatile soyabean is apart of everyone’s life in developed countries [1].The crop is grown on about 6% of the world’s arable land

and since the 1970s; the area in soyabean production hasthe highest increase compared with any other crop [2].Global soyabean production was 17 million metric tonnes(MMT) in 1960 and increased to 313 MMT in 2015.

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Future production is expected to increase more than othercrops, due to expanded production area and higher yields.The USA, Brazil and Argentina dominate global soyabean

production [2]. These three countries produced 83%(276 MMT) of world production in 2015. Most of thesoyabeans (116 MMT) were produced in the United States,with 99 MMT in Brazil and 61 MMT in Argentina.China and India produce most of the soyabeans grown inAsia (19 MMT), while only a few are produced in Europeand Africa [3]. In the USA, soyabean is third in production(maize and wheat are first and second).

Nutritional Value of Soyabean

Soyabean plays an important role in food security because itis a highly nutritious crop. In 100 g (raw green soyabeans),soyabeans supply 446 calories and have 9% water, 30%carbohydrates, 20% total fat and 36% protein. Soyabeansare an exceptional source of essential nutrients, providingin a 100-g serving (raw) high contents of the daily value(DV) especially for protein (36% DV), dietary fibre (37%),iron (121%), manganese (120%), phosphorus (101%) andseveral B vitamins including folate (94%). High contentsexist for vitamin K, magnesium, zinc and potassium [4].Because the soyabean crop is highly nutritious and

versatile it offers resources to address world food issuesthrough current and future utilization practices. Futureproduction is expected to increase due to increaseddemand and with the application of newer genomictechnologies the crop has enormous potential to improvedietary quality for people throughout the world whetherconsumed as a vegetable crop or processed into varioussoyabean food products [2].

Soyabean Types and Growth Phases

To effectively manage soyabean pests, in an integrated pestmanagement (IPM) context, it is important to be familiarwith the soyabean plant and its growth throughout the cropseason. Many decisions that a soyabean grower will makedepend on the type of soyabean variety and the growthstage of the plant [5, 6].Soyabean varieties are grouped into 13 maturity groups,

depending on the climate and latitude for which theyare adapted. These maturity groups are given numbers,with numbers 000, 00, 0 and 1 being adapted to Canadaand the northern United States, and numbers VII, VIIIand IX being grown in the southern USA. Group X istropical. Associated with maturity group is the manner inwhich the stem grows and flowering is initiated. Mostnorthern America adapted cultivars have an indeterminategrowth pattern; the terminal bud continues its vegetativeactivity throughout the growing season and the plantcontinues to add foliage after flowering. Most cultivars inthe southern USA and the tropics have a determinate

growth pattern; vegetative growth ceases after flowering.A primary difference between the two, which influencesIPM decisions, is that the indeterminate cultivars have theability to compensate for leaf loss.For the purpose of managing soyabean pests, growth

stage is the most important criterion because the relation-ship between insect injury and crop damage is dependenton the stage when the injury occurs. Research studiesindicate that injury during the vegetative stages is usuallynot as detrimental to the plant as that during thereproductive stages. The following system is used with ‘V’representing vegetative stages and ‘R’ reproductive stages:

Because soyabean response to insects is dependent ongrowth stage, economic thresholds vary with the stage.Therefore, it is important that growers recognize thesedevelopmental stages.

Cropping Systems

Most soyabeans are grown in a crop rotation sequence,typically with a non-legume such as maize, small grains,sorghum or cotton. The yield of the non-legume isimproved because of the left-over nitrogen from thesoyabean root nodules. In addition, disease, pest andweed problems are reduced in rotations compared withgrowing one crop continuously [1].Soyabeans are also often grown in a double-cropping

system, with two crops being grown in the same year.Winter wheat followed by soyabeans is the most common;snap beans or peas followed by soyabeans is another.

Constraints to Soyabean Production

There are a number of abiotic and biotic constraints thatthat threaten soyabean production by directly reducingseed yields and/or seed quality. Abiotic constraints includeextremes in nutrients, temperatures and moisture. Thesereduce production directly, but also indirectly throughincrease in pathogens and pests [2]. Biotic constraintsconsist primarily of insects, pathogens, nematodes andweeds.

Vegetative stages Reproductive stages

VE: emergence R1: beginning bloomVC: cotyledon+unfolding unifoliate R2: full bloomV1: 1st node trifoliate R3: beginning podV2: 2nd node trifoliate R4: full podV3: 3rd node trifoliate R5: beginning seedV4: 4th node trifoliate R6: full seedV5: 5th node trifoliate R7: beginning maturityVn: Nth node trifoliate R8: full maturity

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Pathogens and pests of soyabeans infect and/or attack allparts of the soyabean plant from roots to seed pods [7].The extent of economic damage depends on the type ofpest/pathogen, plant tissue being attacked, number of plantsaffected, severity of attack, environmental conditions, hostplant susceptibility, plant stress level and stage of plantdevelopment [8].Biotic constraints can result in significant negative

impacts on yield. Crop losses to animal pests, diseasesand weeds in soyabeans average 26–29% globally [9, 10].Weeds are the predominant pest group in soyabeans.Weed competition causes 37% loss of attainable pro-duction while fungal pathogens, bacterial pathogens, virusesand animal pests (insects, mites, nematodes, rodents, birdsand mammals) cause 11, 1, 11, and 11% losses of attainableproduction, respectively. In India, losses in soyabean to theinsect complex were estimated to be 18 and 24% inmonocrop and when intercropped with maize, respectively[11]. Soyabean disease loss estimates for the top tensoyabean producing countries (97.6% of the world’ssoyabean production) indicated that losses were highestdue to the soybean cyst nematode (SCN) (Heteroderaglycines), brown spot (Septoria glycines), charcoal rot(Macrophomina phaseolina) and sclerotinia stem rot(Sclerotinia sclerotiorum) [12].

Soyabean Insect and Disease Classification

Soyabean insects and diseases can be classified by: (1) cropseason (early-, mid- and late-season), (2) plant parts(organs) attacked [root, stem, foliage and fruiting structures(pods)], (3) plant growth stage when attack occurs (VE –

emergence to R8 – full maturity), (4) insect and diseasetaxonomy (insect and disease species) and (5) causal agentsfor the insect and disease damage (bacteria, fungi, oomy-cetes, viruses and nematodes).

Soyabean insects

Soyabeans can be attacked by pests, at any stage from theseedling stage to close to harvest, but are most attractive toinsects from the flowering stage onwards [13]. Insectsdamage soyabeans directly by feeding on the varioussoyabean plant parts and indirectly by transmitting adisease while feeding or predisposing the plant to attackof diseases due to the feeding damage.Based on their importance the insect pests in Brazil are

classified as: (1) key pests, (2) secondary pests (someimportance in restricted areas or occurring too early ortoo late in the crop cycle to cause economic damage),(3) regionally important pests and (4) sporadic pests [14].Globally, there are hundreds of insect species that feed

on the soyabean plant but the majority of them do verylittle damage. According to Hoffman-Campo et al. [15], inBrazil only about 35 insect species are considered as

soyabean pests. All of the plant parts are vulnerable toinsect attack: leaf buds, cotyledons, leaves, stems, nodules,petioles, roots, pods and developing grain.Insect damage to soyabeans in field is manifested various

types of symptoms. These include (1) gaps in the plant standdue to the pruning of roots, wilting plants, tunnelling intothe cotyledon, embryo or hypocotyl due to the feeding ofcoleopteran grubs (larvae) and the seedcorn maggot;(2) holes in leaves or skeletonized leaves due to thefeeding of defoliating insects primarily Lepidoptera andColeoptera; (3) leaves are distorted and discoloured due tothe feeding of aphids and spider mites and (4) pods aredamaged by the feeding of the bean leaf beetle, pod borersand stink bugs [16].Traditionally insects associated with crops, such as

soyabean, are grouped according to their feedingbehaviour [17]. This classification allows damage estimates,appropriate sampling methods and even preliminaryidentification [4].Based on their feeding behaviour they are placed in four

groups:

(1) root and below ground feeders,(2) stem feeders,(3) foliage feeders and(4) pod feeders.

Root and below ground feeders (Table 1)Insects in three orders, Coleoptera, Diptera and Hemipteraare considered to be root and below ground feeders. Theyfeed on soyabean roots and seed.Grape colaspis is a pest in North America. Adults feed

on soyabean trifoliate leaves and larvae prune the roots androot hairs of young seedlings. The grubs move up in the soilto near the surface in late May, remove fine roots and gouge‘channels in the roots of soyabean plants’. The grubs aresmall white larvae with a brown head capsule and neckshield. Damaged seedlings have few lateral roots and theunderground stem may show feeding on the bark. Seedlingsmay die or be stunted by the feeding of the insect [18].White grubs: White grubs are polyphagous pests and

attack soyabeans in North America and Brazil (Table 1).The larvae are white and ‘C’-shaped. The true white grubPhyllophaga can be identified by having two, parallel rows ofstiff bristles on the underside of its tail end. Annual whitegrubs Cyclocephala lurida, lack this pattern of bristles [19].Injury to soyabean from white grubs is uncommon.However, second and third-instar true white grub larvaecan cause damage to soyabean by feeding on roots andcausing stand loss.True white grubs typically have life cycles that span 3–4

years (known as semivoltine) while the annual white grub isunivoltine. These grubs are not common in soyabean, but ininfested fields, larvae can be found feeding on rootsthroughout the growing season. The adults fly to and feedon foliage of deciduous trees and, during spring, will drop to

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the ground to deposit eggs. Larvae will feed in the rootzone just a few inches from the soil line.Wireworms: Although economic damage to wire-

worms in North America is rare, when they are aproblem, they can be very destructive and difficult tocontrol. They are usually found attacking soyabeans plantedin fields that have been in sod for several years, or thesecond year following sod [20]. Wireworms can feed onand damage one or more portions of a soyabean seed, orcan completely hollow it out leaving only the seed coat.Wireworms may also cut off small roots or tunnel into theunderground portions of young soyabean plants. Theseplants will appear stunted or wilted [21]. Since the life cycleof some wireworm species may last from 4 to 6 years,larvae may damage successive crops [22].Seedcorn maggot: Seedcorn maggots may destroy

soyabean seeds before they germinate or kill young plantsbefore they emerge from the soil. Maggots will also feed ondeveloping cotyledons, which can destroy the growing tips.Damage is most likely to occur if germination is delayeddue to cool wet weather [23]. Disturbed soil withdecaying organic matter, such as manure or green plantmaterial (cover crop or weeds), is highly attractive tofemale flies for oviposition. Seedcorn maggot feeding canresult in direct loss by destroying the seed and causing standloss [22].Brown root stink bug is a pest of soyabean in South

America. It has been intensively studied in Brazil [24]. Bothnymphs and adults suck the sap of plants from the roots andcause withering and even plant death. They often occur infields previously in pastures. In Mato Grosso, Brazil,120 000 ha of soyabean was infested with brown root

stink bug in 1999 resulting in yield losses ranging from 20 to80%. It is most common in sandy soils but also occurs inclay soils. Damage symptoms include a reduction in plantheight and reduced stand due to dead plants, and areduction in the number of pods per plant. Yield losseswere greatest when attack occurred in the early stages ofplant development.Bean leaf beetle – a vector of bean pod mottle virus

(BPMV) – is a soyabean pest in North America. The larvaelive underground, feeding on soyabean roots, particularlynodules. Bean leaf beetle adults feed on the above groundpart of soyabean such as cotyledon, leaves and pods (https://wiki.bugwood.org/NPIPM:Cerotoma_trifurcata).

Stem feeders (Table 2)Insects in four orders attack soyabean stems. The stemfeeders bore within the stem leaving feeding tunnels(Coleoptera, Diptera and Lepidoptera) or pierce thestems and suck phloem sap from within the stem(Hemiptera).Soybean stem borer is a pest in Asia. The small, bluish

grey beetle lays its eggs in the petioles of soyabean leaves.The larvae tunnel down to the base of the plants, eventuallygirdling the stem just above the soil line. Lodging occurs asthe plants mature, making harvest difficult and reducingyield.Soybean stem flies: Melanogromyza sojae and

Ophiomyia phaseoli are widely distributed globally. M. sojaeis an important soyabean pest in Africa and Asia but doesnot occur in North America and O. phaseoli occurs in allregions except in South America. M. sojae flies lay eggs onundersides of leaves. After hatching from the egg, yellowish

Table 1. Pests of soyabean and their geographical distribution: insects – root and below ground feeders

Insects Asia Africa Europe N. America S. America Australia

Root and below ground feedersGrape colaspisColaspis brunnea X(Coleoptera: Chrysomelidae)White grubsPhyllophaga spp. X(Coleoptera: Scarabaeidae)Southern masked chaferCyclocephala lurida X(Coleoptera: Scarabaeidae)WirewormsMelanotus spp. XAgriotes mancus XLimonius dubitans X(Coleoptera: Elateridae)Seedcorn maggotDelia platura X(Diptera: Anthomyiidae)Brown root stink bugS. castanea X(Hemiptera: Cydnidae)Bean leaf beetleC. trifurcata X(Coleoptera: Chrysomelidae)

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maggots mine through the leaf tissue towards the mid vein.From here, they work their way down the leaf petiole intothe stem where it feeds on the pith. If the infected stem isopened by splitting, a distinct zigzag reddish tunnel can beseen with maggots or pupae inside it. The maggots feed oncortical layers of the stem, and feeding damage may extendto the taproot. Before pupation, which takes place insidethe stem, the larva makes an exit hole for the emergence ofthe adult, through the stem’s xylem and phloem tissue. It isthis damage to the soyabean plant’s vascular tissue thataffects the plant’s growth and reduces yield [25].Three-cornered alfalfa hopper, a North American

pest, is a membracid that prefers leguminous plants such asalfalfa, soyabean, bean, cowpea and sweet clover (https://soybeans.ces.ncsu.edu/three-cornered-alfalfa-hopper/).Adults and late instar nymphs feed on the plant sap bypiercing the stem with their needle-like mouthparts andextracting plant juices a few inches above the soil surface.Feeding results in the girdling of the main stem. Typically, aninsect will repeatedly feed in a ring-like fashion at the samelocation on the stem. As the plant grows, a swollen callus

generally develops on the stem at the feeding site. Stemsmay break at the site of the girdle. On large plants, lateralbranches, leaf petioles and pod stems are often girdled in asimilar fashion. Stem injury on small plants may ultimatelycause plants to break and lodge [26].Kudzu bug: The kudzu bug is an invasive pest that was

introduced into North America from Asia (India and China)where it is a native. In the southeastern United States, it wasfirst observed in northeastern Georgia in 2009. It has sincespread to several neighbouring states. It is the onlyrepresentative of the family Plataspidae in North America.The insect taps through the veins of plants to reach the

phloem, using piercing–sucking mouthparts. As a result,injury to plants likely results from nutrient and moistureloss, rather than a direct loss of biomass from removal ofplant tissue. On soyabeans, the kudzu bug adults andnymphs feed on stems. Excessive kudzu bug feedingnegatively impacts soyabean yield by reducing pods perplant, reducing beans per pod, and/or reducing seed size. In2011, yield losses of up to 47% were recorded in Georgiaon untreated beans on a research station near Midville;

Table 2. Pests of soyabean and their geographical distribution: insects – stem feeders

Insects Asia Africa Europe N. America S. America Australia

Stem feedersSoybean girdle beetleObereopsis brevis X(Coleoptera: Cerambycidae)Soybean stem borerDectes texanus texanus X(Coleoptera: Cerambycidae)Lucerne crown borerZygrita diva X(Coleoptera: Cerambycidae)Cascudinho da sojaMyochrous armatus X(Coleoptera: Chrysomelidae)Brazilian soybean stalk weevilSternechus subsignatus X(Coleoptera: Curculionidae)Soybean stem flyM. sojae X X X X X(Diptera: Agromyzidae)Soybean stem flyOphiomyia phaseoli X X X X X(Diptera: Agromyzidae)Three-cornered alfalfa hopperSpissistilus festinus X(Hemiptera: Membracidae)Kudzu bugMegacopta cribraria X X X(Hemiptera: Plataspidae)Common plataspid stinkbugM. punctatissima X(Hemiptera: Plataspidae)Lesser cornstalk borerElasmopalpus lignosellus X X(Lepidoptera: Pyralidae)Broca das axilasCrocidosema aporema X(Lepidoptera: Tortricidae)

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only two kudzu bugs were found at this location theprevious autumn [27].The Lesser Cornstalk Borer (LCB) is a lepidopteran

species of snout moth. It is found from the southernUnited States to Mexico, Central America andSouth America (Colombia, Venezuela, Brazil, Peru,Argentina and Chile) [28].The LCB larva is bluish-green with brown or purple

bands. When disturbed the larva thrashes wildly. Larvaebuild a distinctive sand-covered silken tube that is attachedto the host plant. LCB damage to soyabean is first noticedas wilting, dead or lodged plants. When seedlings areuprooted, damage at the soil line may consist of an entryhole, girdling or multiple feeding sites. Splitting the stemssometimes reveals that the larva tunnelled into the plant. Ifplants are older when attacked, LCB feeding may not killthem and damage shows up later when stems break at thesoil line from previous injury. This injury can be confusedwith that of three-cornered alfalfa hopper but LCB injuryalways occurs at the soil line whereas three-corneredhopper injury occurs higher up on the main stem or lateralbranches [29].The life cycle can take only 3 weeks and multiple

generations occur, but soyabean becomes less vulnerableto attack as the plant grows and the stem thickens. LCBthrives on hot, dry sandy soils because the larval cuticle or‘skin’ is able to retain body water much better than mostinsects. As a result, the LCB can thrive when conditionsare too extreme for the beneficial insects that normallycontrol it.

Foliage feeders (Table 3)The ‘foliage feeders’ refers to a broad category whichconsists of a number of insect orders including Coleoptera,Diptera, Hemiptera, Lepidoptera, Orthoptera andThysanoptera, and a mite species (Acarina: Tetranychidae),that feed on soyabean foliage. The group has mouthpartsthat determine the type of feeding damage caused. Thelepidopterous larvae, coleopterous larvae and adults andorthoptera nymphs and adults, have chewing mouthpartswhich are used to defoliate plants. The Diptera larvae havecephalopharyngeal skeleton mouthparts, the Hemipteranymphs and adults and mites have piercing–suckingmouthparts that penetrate the foliage and Thysanopterahave rasping–sucking mouthparts.Soyabeans are able to compensate for large amounts of

foliage loss due to insect feeding and often little yield loss isobserved [30]. Soyabeans can tolerate up to 33% leaf loss(providing terminal and auxiliary buds are not attacked)without yield loss. Soyabean plants not only continue to putout new leaves at the top to compensate for the feedingbut also leaves positioned below the feeding injury sitesactually grow larger, increasing surface area, since they aregetting more sunlight through the canopy. Soyabeans set alarge number of reserve pods and can compensate forinsect damage during early podding by diverting energyto fill these reserve pods. However, the most critical stage

for soyabeans is beginning bloom (R1) to full pod (R4),when seed development is highly dependent on photo-period [16].Chrysomelidae: Among the beetle species attacking

soyabeans, chrysomelids are the most important in Brazil[31]. Several chrysomelids are soyabean pests in Asia,North and South America and Australia. Of the Diabroticaspecies, the banded cucumber beetle, Diabrotica balteataand the spotted cucumber beetle D. undecimpunctata (alsoknown as the corn rootworm) are soyabean defoliators inNorth America and the cucurbit beetle, D. speciosa is asoyabean leaf feeder in Brazil. Diabrotica are polyphagousfeeding on a wide range of hosts in the families Asteraceae,Cucurbitaceae, Fabaceae, Poaceae and Solanaceae. Adultsfeed on rice foliage while the larvae feed on plant roots.Leaf miners, Liriomyza sativae and Liriomyza

trifolii: These are a few of the dipterans feeding onsoyabean foliage. They are widely distributed except forthat L. sativae does not occur in Europe. They arepolyphagous pests of many vegetable and flower crops.Their preferred hosts tend to be in the Cucurbitaceae,Fabaceae and Solanaceae families [32].Adults and larvae damage the plant foliage. Feeding

punctures appear on the upper side of the leaves as whitespeckles 0.13–0.15 mm in diameter. Oviposition puncturesare smaller (0.05 mm) and are more uniformly round.Foliage punctures caused by female adults during the acts ofoviposition or feeding may cause a stippled appearance onfoliage, but this damage is slight compared with the leafmining activity of larvae. The irregular mine increases inwidth from about 0.25 mm to about 1.5 mm as the larvamatures. Larvae are often easily visible within the minewhere they remove the mesophyll between the surfacesof the leaf. Their faecal deposits are also evident in themines [33].Whiteflies: Among the whitefly species the sweet

potato whitefly and the silver-leaf whitefly (SLW) areglobally distributed foliage-feeding pests. The SLWB-biotype is a pesticide-resistant strain of the whiteflyBemisia tabaci. The SLW is a major global pest ofhorticultural and agricultural crops throughout the world,except in Antarctica [34] and is highly resistant to mostcurrent pesticides.The SLW, a polyphagous pest of agricultural importance

throughout the world, can secrete large amounts of stickyhoneydew. Although the whitefly may cause some croplosses, simply by sucking sap when they are very numerous,the major harm they do is indirect. Firstly, like many othersap-sucking Hemiptera, they secrete large amounts ofhoneydew that support unsightly or harmful infestationsof sooty mould. Adult females produce more honeydewthan other stages and nymphs produce more honeydewwhen feeding on stressed plants. Honeydew is not a majorproblem, but the sooty mould, which develops onhoneydew shields, leaves from sunlight and reducesphotosynthesis. Secondly, they inject saliva that may harmthe plant more than either the mechanical damage of

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Table 3. Pests of soyabean and their geographical distribution: insects and mites – foliage feeders

Insects and mites Asia Africa Europe N. America S. America Australia

Foliage feedersWestern striped cucumber beetle – Acalymma vittatum(Coleoptera: Chrysomelidae) XBanded cucumber beetleD. balteata X(Coleoptera: Chrysomelidae)Cucurbit beetleD. speciosa X(Coleoptera: Chrysomelidae)Spotted cucumber beetleD. undecimpunctata X(Coleoptera: Chrysomelidae)Cascudinho verdeMaecolaspis calcarifera X(Coleoptera: Chrysomelidae)Red-shouldered beetleMonolepta australis X(Coleoptera: Chrysomelidae)Bean leaf beetleC. trifurcata X(Coleoptera: Chrysomelidae)Locust leafminerOdontota dorsalis X X(Coleoptera: Chrysomelidae)Mexican bean beetleE. varivestis X(Coleoptera: Coccinellidae)Imported longhorn weevilCalomycterus setarius X X(Coleoptera: Curculionidae)Besouro marromAracanthus mourei X(Coleoptera: Curculionidae)Blister beetleEpicauta pestifera X(Coleoptera: Meloidae)Blister beetleE. lemniscata X(Coleoptera: Meloidae)Japanese beetleP. japonica X X X(Coleoptera: Scarabaeidae)American serpentine leafminerL. trifolii X X X X X(Diptera: Agromyzidae)Leaf minerL. sativae X X X X X(Diptera: Agromyzidae)Sweet potato whitefly B. argentifolii (B. tabaci biotype B)(Hemiptera: Aleyrodidae) X X X X X XSilverleaf whiteflyB. tabaci X X X X X X(Hemiptera: Aleyrodidae)Soybean aphidA. glycines X X X X(Hemiptera: Aphididae)Green miridCreontiades dilutus X(Hemiptera: Miridae)Leaf folderHedylepta indicata X(Lepidoptera: Crambidae)Leaf folder

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Table 3. (Continued)

Insects and mites Asia Africa Europe N. America S. America Australia

Nacoleia vulgalis X(Lepidoptera: Crambidae)Bean leafrollerOmiodes diemenalis X X X(Lepidoptera: Crambidae)Saltmarsh caterpillarEstigmene acrea X(Lepidoptera: Erebidae)Green cloverwormPlathypena scabra X(Lepidoptera: Erebidae)Bihar hairy caterpillarSpilosoma obliqua X(Lepidoptera: Erebidae)Leaf minerAproaerema modicella X X(Lepidoptera: Gelechiidae)Australian soybean mothA. simplexella X X(Lepidoptera: Gelechiidae)Silver-spotted skipperEpargyreus clarus X(Lepidoptera: Hesperiidae)Velvetbean caterpillarA. gemmatalis X X(Lepidoptera: Noctuidae)Green semilooperChrysodeixis acuta X(Lepidoptera: Noctuidae)Tobacco looperC. argentifera X(Lepidoptera: Noctuidae)Green looper caterpillarC. eriosoma X X X X(Lepidoptera: Noctuidae)Soybean looperC. includens X X X(Lepidoptera: Noctuidae)Soybean looperThysanoplusia orichalcea X X X X(Lepidoptera: Noctuidae)Green semilooperDiachrysia orichalcea X(Lepidoptera: Noctuidae)Green semilooperGesonia gemma(Lepidoptera: Noctuidae)Soybean looperP. includens X X(Lepidoptera: Noctuidae)Southern armywormS. eridania X X(Lepidoptera: Noctuidae)Beet armywormS. exigua X X X X X(Lepidoptera: Noctuidae)Autumn armywormS. frugiperda X X X X(Lepidoptera: Noctuidae)Yellow-striped armywormS. ornithogalli X(Lepidoptera: Noctuidae)Common cutworm

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feeding or the growth of the fungi. However, by far theirmajor importance as crop pests is their ability to transmitplant diseases [13].Feeding by the SLW manifests itself in several ways [13]:

(1) SLW can reduce plant vigour and yield by the sheerweight of numbers removing large amounts of plantphotosynthate from the leaves; (2) severe infestations onyoung plants can stunt plant growth and greatly reduce acrop’s yield potential; (3) later infestations can reduce thenumber of pods set, seed size and seed size uniformity, thusreducing yield and quality and (4) in heavily infestedsoyabeans, both pods and seeds are often unusually pale.While seed colour is unlikely to be of concern in grainsoyabeans (harvested seeds being naturally pale), pod andseed discoloration are a major marketing problem wherepods are picked green (e.g. vegetable soyabeans). As a rule,the impact of SLW is worst in drought stressed crops.The SLW is also a vector of a virus of the carlavirus group

on soyabean. This virus is responsible for the diseaseknown as ‘soyabean stem necrosis’. Soyabean plantsinfected with this virus display necrotic stems, which assymptoms progress may kill the plant [34].The soybean aphid, a native of Asia and invasive pest,

was first observed in the USA in 2000 [35]. It also occurs inEurope and Australia but is not known to occur in Africaand South America (Table 2). In North America Rhamnuscathartica (buckthorn) is the primary host. Soyabean is themost important secondary or summer host [36].Aphids have piercing–sucking mouthparts that suck

juices and nutrients from the plant. Removal of plant sapby feeding on the leaves causes stunting, leaf distortion andreduced pod set. An additional threat is the ability of theaphid to transmit soybean viruses [37].Honeydew excreted by soybean aphids leads to the

development of sooty mould that restricts photosynthesis[2]. Yield loss due to soybean aphid feeding is greatestwhen soyabeans are in the early R stages (R1−R2), thestages when flowers abort and impact pod establishment.Peak infestations during the pod fill stage (R3), and beyond,can result in smaller seed size and a reduction in seedquality.An economic analysis of the impact on soyabean

production predicted that, without effective plant

resistance, US$3.6 to $4.9 billion in soyabean productioncould be lost annually depending on the cost of insecticideapplications, the size of the aphid outbreak and the priceelasticity of the soyabean supply [38].Lepidopteran defoliators: There are numerous lepi-

dopteran species that are key or secondary defoliators ofsoyabean plants. These include leaf folders, leafrollers, leafminers, loopers, semi-loopers, armyworms, cutworms,various and ‘caterpillar’ species. A few grasshopper andthrips species are occasional pests feeding on soyabeanfoliage (Table 3).Velvetbean caterpillar: It is considered as the ‘main’

soyabean pest in Brazil [39] and one of the most importantdefoliators occurring in soyabeans from Argentina to thesoutheastern United States [40]. It is the most damagingfoliage-feeding pest of soyabean in Florida and the south-eastern USA [41].The occurrence of this species is restricted to the

American continent, where if feeds on various crops,especially soyabean [42]. The velvetbean caterpillar is apermanent inhabitant of tropical America and migratesnorthwards into the southeastern United States every year.The caterpillar overwinters in the southern tip of Floridaand moves north during the summer months. Anticarsiagemmatalis is an annual problem from June throughSeptember in Florida, Georgia and Alabama.Velvetbean caterpillars cause damage by consuming

foliage. To complete its larval development, the velvetbeancaterpillar consumes from 85 to 150 cm2 of leaf area butthe majority of this consumption is performed by larvaefrom the 4th to 6th instar, which are caterpillars>1.5 cm [34].Newly hatched larvae strip the leaf, beginning with the

lower epidermis and mesophyll. They continue feeding untilthe end of the second instar, eating all the soft leaf materialand leaving only the veins intact [43]. Eventually thevelvetbean caterpillar consumes the entire leaf. Once theupper leaves and lower leaves have been consumed, foliagein the middle and lower canopy is consumed and completedefoliation may result [44]. The velvetbean caterpillar mayalso attack tender stems, buds and small bean pods.Soybean thrips differ from the other foliage feeders in

the way they feed on leaves. Thrips mouthparts make them

Table 3. (Continued)

Insects and mites Asia Africa Europe N. America S. America Australia

S. litura X X(Lepidoptera: Noctuidae)GrasshoppersMelanoplus spp. X(Orthoptera: Acrididae)Soybean thripsNeohydatothrips variabilis X(Thysanoptera: Thripidae)Two-spotted spider miteT. urticae X X X X X X(Acarina: Tetranychidae)

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unique in that they rasp and puncture plant cells then suckup the exuding sap. Their appearance, biology and feedingdamage has been described in [45].Thrips are minute, slender-bodied insects ranging from

0.8 to 5 mm in length. The immatures are yellow, whileadults are black with yellow bands. Their wings, whenpresent, are fringed with long hairs. Although rarelynoticed, thrips are probably the most numerous insectsin soyabean.The adult female inserts oblong eggs singly into the leaves

of the plant upon which she feeds. Young thrips go throughfour wingless stages between hatching and adulthood. Anentire life cycle requires only 2–4 weeks. Thrips are presentthroughout the summer in the USA.Thrips make tiny, linear, pale-coloured scars on soya-

bean leaves where they penetrate individual leaf cells andfeed on the contents. They usually feed on the undersidesof leaves, much of which occurs along the veins. Whenleaves are heavily infested, the feeding scars may be sonumerous that a mottling look appears along and betweenthe leaf veins and leaves may become crinkled in appear-ance. Another indication of their activity is the presence ofblack ‘tar spots’ on the leaves. This is thrips excrement andthe descriptive name is quite accurate.Soyabean is particularly susceptible to thrips damage

early in the growing season from growth stages VE to V6.Although thrips are a common pest of soyabeans in theUnited States, they rarely cause economic damage.Nevertheless, yields may be reduced if plants are undermoisture stress and thrips populations are high.Two-spotted spider mites are globally distributed

throughout the world (Table 3). During feeding the mitespenetrate the plant foliage/leaves with their mouth styletsand suck out the cell contents. The result of this damage toleaf tissue is reduced chlorophyll content and reducedphotosynthesis, carbon dioxide assimilation and transpira-tion. Feeding by the two-spotted spider mite causes palespots to appear on leaves. As infestations become moresevere, leaves appear bronzed or silvery, become brittle,and may fall prematurely. The mites spin webbing, whichcan cover all the surfaces of the plant. Plants can be rapidlykilled this mite (https://www.cabi.org/isc/datasheet/53366).

Pod feeders (Table 4)Insects in the orders Coleoptera (beetles), Lepidoptera(armyworms) and Hemiptera (stink bugs) damage soyabeanpods. The Coleoptera larvae and adults and Lepidopteralarvae have chewing mouthparts with which they devourthe pods and green beans within. Both the stink bugnymphs and adults have piercing–sucking mouthparts forremoving plant fluids [16].Among the lepidopterous pod feeders, the lima bean pod

borer (Maruca vitrata), pod borer (Helicoverpa armigera)and the pea pod borer (Etiella zinckenella) are widelydistributed globally.Legume pod borer is considered the most serious

pest of food legumes in tropical Asia, sub-Saharan Africa,

South America, North America, Australia and the Pacific[46]. Its bionomics and management on cowpea have beenreported [47]. It is an invasive species, and a pantropicalinsect pest (Table 4) of leguminous crops e.g. cowpea,pigeonpea, mung bean, common bean, soyabean, adzukibean, groundnut, hyacinth bean, and field peas, countrybean, broad bean, kidney bean and lima bean. The legumepod borer is a serious pest of grain legumes in the tropicsand sub-tropics because of its extensive host range, anddestructiveness.The importance of it as a pest on grain legumes results

from its early establishment on the crop. The larvae webthe leaves and inflorescence, and feed inside flowers, flowerbuds and pods. This typical feeding habit protects the larvaefrom natural enemies and other adverse factors, includinginsecticides. The successful establishment of this pest at theflower bud stage is significant in relation to subsequentdamage, reduction in grain yield and efficiency of control.Third to fifth-instar larvae are capable of boring into thepods and consuming the developing grains.Lima bean pod borer occurs in Asia, sub-Saharan

Africa, South America, North America, Australia andEurope. Although it has been reported on several legumecrops, it causes significant yield losses in lentil, peas andsoyabean [48]. Infestation of soyabean plants usually startslate in the season. The larvae feed on floral buds, flowersand pods by making rough and irregular incisions. The podsmay have several entry holes. The larvae feed on the seedsinside the pods. Often the damaged pods and inflorescenceshow light coloured frass and loosely spun webs. InIndonesia, E. zinckenella can cause severe damage to thepods and yield losses can reach 80% [49].Helicoverpa species: Three Helicoverpa species are

pod feeders (Table 4). The pod borer H. armigera occurs inall regions, recently invading North America (Florida). Thenative budworm H. punctigera is a pest in Australia andthe American cotton bollworm H. zea attacks soyabeanpods in North and South America. All have similar feedinghabits.The gram pod borer, H. armigera, is a polyphagous and

highly mobile insect and it is a pest of economic importanceon many agricultural and horticultural crops. It is a majorpest on a number of crops, including cotton, tobacco, corn(maize), sorghum, sunflower, soyabean, lucerne and pepper[48]. It has been recorded on 180 cultivated and wild plantspecies in at least 45 families. Occasionally it causessignificant yield losses in mungbean, vegetable soyabean,chickpea and pigeon pea.The neonate larvae feed on the surfaces of leaves or

floral buds. However, the grown-up larvae prefer to feed onthe contents of reproductive parts such as floral buds,flowers and young fruits. The larvae make the holes onthese reproductive parts and feed inside by thrusting theirhead inside; hence, the holes are circular and oftensurrounded by faecal pellets. Later, the larva feeds onmost of the inner contents of the pod and damaged podsmay become deformed [48].

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Table 4. Pests of soyabean and their geographical distribution: insects – pod feeders

Insects Asia Africa Europe N. America S. America Australia

Pod feedersBean leaf beetleC. trifurcata X(Coleoptera: Chrysomelidae)Legume pod borerM. vitrata X X X X X X(Lepidoptera: Crambidae)Gram pod borerH. armigera X X X X X X(Lepidoptera: Noctuidae)Native budwormH. punctigera X(Lepidoptera: Noctuidae)American cotton bollwormH. zea X X(Lepidoptera: Noctuidae)Tobacco budwormHeliothis virescens X X(Lepidoptera: Noctuidae)Southern armywormS. eridania X X X(Lepidoptera: Noctuidae)Garden armywormS. latifascia X X(Lepidoptera: Noctuidae)Lima bean pod borerE. zinckenella X X X X X X(Lepidoptera: Pyralidae)Green stink bugAcrosternum hilare X(Hemiptera: Pentatomidae)Southern green stink bugN. viridula X X X X X X(Hemiptera: Pentatomidae)Neotropical brown stink bugE. heros X(Hemiptera: Pentatomidae)Brown stink bugE. servus X(Hemiptera: Pentatomidae)Redbanded shield bugP. grossi X X X(Hemiptera: Pentatomidae)Redbanded stink bugP. guildinii X X(Hemiptera: Pentatomidae)Large brown bean bugRiptortus serripes X(Hemiptera: Alydidae)Small brown bean bugMelanacanthus scutellaris X(Hemiptera: Alydidae)Brownshield bugDictyotus caenosus X(Hemiptera: Pentatomidae)Green-belly stink bugD. furcatus X(Hemiptera: Pentatomidae)Green and brown stink bugEdessa meditabunda X(Hemiptera: Pentatomidae)Brown marmorated stink bugHalyomorpha halys X X X X

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H. armigera is an important soyabean pest in Australiawhere it can severely damage all crop stages and all plantparts of soyabeans. Of the summer legumes, soyabeans arethe most attractive to Helicoverpa during the vegetativestage and can even be damaged during the seedling stage. Insub-coastal and inland southern Queensland, summerlegumes are at greatest risk from H. armigera frommid-December onwards [13].Stink bugs: While pod-sucking bugs start breeding as

soon as they move into flowering crops, nymphs must feedon pods to complete their development [13]. Both adultsand nymphs have piercing–sucking mouthparts for remov-ing plant fluids. Stink bugs feed directly on pods anddeveloping seeds. However, their damage is difficult toassess because their mouthparts leave no obvious feedingscars on the surface of the pod. Instead, they inject enzymesinto the seeds, causing the seed to shrivel [13]. The feedingwound provides an avenue for diseases to enter into thepod.Seeds damaged by stink bugs during early pod-fill are

often lost at harvest, or are graded out post-harvest, as theyare lighter than undamaged seeds. Crops remain suscep-tible to late bug damage until the pods harden just prior toharvest [16]. Indirect effects can include delayed maturity(green bean syndrome) of injured plants, though stink bugsare not the only cause for green bean syndrome.There are many stink bug species feeding on soyabeans

globally [50]. The list in Table 4 is a representation of theimportant species in the six regions of the world. Thesouthern green stink bug Nezara viridula is widely dis-tributed and an important pest of soyabeans globally.N. viridula, the Neotropical brown stink bug Euschistusheros, and the redbanded stink bug Piezodorus guildinii, aremajor pests in Brazil and represent 98% of the total stinkbug population [51]. The brown marmorated stink bug(BMSB) is an invasive pest occurring in Asia, Europe andNorth America with potential to spread to other regions.Southern green stink bug, a native to Ethiopia, is a

cosmopolitan and highly polyphagous pest species feedingon more than 52 documented host plants, includingornamentals, weeds and cultivated crops, in 30 plantfamilies [52]. Although it causes economic damage tomany crop species, it mainly feeds on legumes. It is aninvasive pest and was first reported in northeastern Brazil in2001 [53]. This species is the most damaging pod-suckingbug in soyabeans due to its abundance, widespreaddistribution, rate of damage and rate of reproduction.Nymphs are less damaging than adults. While first instar

nymphs cause no damage, subsequent instars are progress-ively more damaging, with the fifth and final instar beingnearly as damaging as adults are.The damage symptoms are similar to other pod bugs,

causing drying of shoots, shrivelled pods and seeds. Bugdamaged seeds are frequently discoloured, either directlyor due to the yeast-spot disease, Nematospora coryli [54],which gains entry when pods are pierced by bugs.It can even damage seeds in ‘close-to-harvest’ pods (i.e.

pods that have hardened prior to harvest). Seeds damagedin older pods are blemished and difficult to grade out,reducing harvested seed quality, particularly that destinedfor human consumption (edibles). Damage to young podscauses deformed and shrivelled seeds and reduce yield.Bug-damaged seeds have increased protein content but ashorter storage life (due to increased rancidity). Bugdamage also reduces seed oil content.Neotropical Brown Stink Bug is a Neotropical

pentatomid occurring in South America. Most reportsrefer to its distribution in Brazil where it is a majorcomponent of the pentatomid-pest complex on soyabean.Initially considered a secondary pest, E. Heros has increasedin numbers and may inflict severe damage to soyabean. Inthe southern-most state of Rio Grande do Sul (RS) in BrazilE. heros is now the most abundant species of pentatomid onsoyabean, reaching over 80% of the total number of stinkbugs collected in Passo Fundo, RS (A. R. Panizzi, personalcommunication).Beyond soyabean, this insect feeds on several other

plants (in 11 families) in Brazil, including species ofLeguminosae, Fabaceae, Solanaceae, Brassicaceae andCompositae [55]. Even though it is polyphagous and,therefore, able to colonize alternate hosts during the mildwinter of northern Paraná state, E. heros was found tooverwinter underneath dead leaves in this area. This bug isknown to accumulate lipids during overwintering that allowsurvivorship during non-feeding periods, and to breakdormancy with the start of favourable weather conditions.During summer, with the availability of the great number ofweeds associated with the soyabean crop, this bug alsofeeds on some weeds.Redbanded stink bug has a wide Neotropical distri-

bution (Table 4) that ranges from Argentina to thesouthern United States [50]. Since the late 1970s, theredbanded stink bug has replaced the southern green stinkbug as the principal stink bug pest in portions of Brazil [56].Redbanded stink bugs appear to be more adapted towarmer climates.

Table 4. (Continued)

Insects Asia Africa Europe N. America S. America Australia

(Hemiptera: Pentatomidae)Neotropical red-shouldered stink bugThyanta perditor X X(Hemiptera: Pentatomidae)

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It has existed in Florida (USA) for many years withoutbeing a serious pest. However, it has recently become amajor pest of soyabean in Alabama, Georgia, Louisiana,Mississippi, South Carolina and Texas [55]. It was firstidentified as a pest of Louisiana (USA) soyabean in 2000[57]. In a survey conducted in Louisiana the redbanded stinkbug comprised the largest percentage (54%) of the totalstink bug complex collected at five survey sites followed byN. viridula (27%), and, Euschistus servus (7%).Compared with N. viridula, P. guildinii feeds on fewer plant

species, being confined mostly to legumes (Fabaceae) [58].Plants of the genus Indigofera seem to be preferred [59].However, other species of cultivated and non-cultivatedplants of different families are at various times used by thispentatomid, either as a source of nutrients or water, or asshelter. The list of plants on which P. guildinii has beenrecorded in the neotropics includes 49 plant speciesbelonging to 22 families, of which 24 species wereconsidered reproductive hosts.Studies in Argentina have shown that the redbanded

stink bug has the greatest capacity to damage soyabeanamong all South American phytophagous stink bugs [60].P. guildinii feeding causes reductions in yield and seed qualityand foliar retention. Galileo and Heinrichs [61, 62]evaluated redbanded stink bug effects on soyabean podproduction seed quality in Brazil. The bugs were infested atzero, two, four, six, and ten insects/1.5 row ft. during thegrowth stages R2−R4, R5, R6−R7 and R2−R7. Nosignificant reduction in yields was detected at two-tenstink bugs/1.5 row ft. during R2−R4 growth stages. Duringthe R5 growth stage, only two stink bugs/1.5 row ft.significantly reduced yields. Infestations during R6−R7growth stages required six stink bugs/1.5 row ft. tosignificantly reduce yields [60].Significant reductions in seed production only occurred

when ≥four redbanded stink bugs/1.5 row ft. were infestedduring R2−R7 growth stages. All treatments had signifi-cantly more damaged seed compared with the non-infestedcontrol during all growth stages except for R2−R4. Percentof seed damaged ranged from 39 (two insects/1.5 row ft.)to 72% (10 insects/1.5 row ft.) [62].In Brazil, delayed soyabean maturity (foliar retention) has

been associated with redbanded stink bug infestations innumerous reports. Panizzi et al. [63] reported thatsoyabean retained green leaves when redbanded stinkbugs infested soyabean during pod development and podfill stages (R3−R6). Heinrichs [64] and Galileo andHeinrichs [65] reported excessive green foliage retentionwhen stink bug populations were ≥eight insects/3 ft. rowduring early seed development, but similar populations atR6 did not delay maturity.Brown marmorated stink bug also known simply as

the ‘stink bug’, is a native to China, Japan, Korea and Taiwan[66]. Currently it is widespread in Europe, and recently hasbeen found in South America [67] (Table 4). In Japan it is apest to soyabean and fruit crops. In the USA, the BMSBfeeds on a wide range of fruits, vegetables and other host

plants including peaches, apples, green beans, soyabeans,sweet corn, cherries, raspberries and pears [68]. Aninvasive pest, the BMSB was accidentally introduced inthe United States from China or Japan. It is believed to havehitched a ride as a stowaway in packing crates or on varioustypes of machinery.The (BMSB), which was first identified in 2001 in

Allentown, PA, USA, was found infesting soyabean fieldsin parts of Virginia in 2011 [69]. The BMSB, similar to thenative stink bug species, feeds directly on developingsoyabean pods and seeds. If the damage occurs very earlyin seed development, pods will be flat and brown, but willstill be attached to the plant and easy to see. If damageoccurs later in seed development, pods will appear yellowand speckled, and opening the pod will reveal damaged,crinkled, stained seed. One visual cue of stink bug damageto soyabean crops is the ‘stay green’ effect, where damagedsoyabean plants stay green late into season, while otherplants in the field die off normally. One can usually tell that asoyabean field is infected because stink bugs are known fortheir ‘edge effect’, in which they tend to infest crops 30–40ft. from the edge of the field.Heavy infestations also seem to be associated with fields

with wooded borders, especially if there are concen-trations of the invasive weed, Tree-of-Heaven (Ailanthusaltissima). Both BMSB and Tree-of Heaven are native toChina and other parts of Asia. The BMSB seems to bestrongly attracted to that host, especially when the treesare putting out their seed clusters. Not coincidently, thenorth-central piedmont area of Virginia, where the highestdensities of BMSB are found in soyabean, is the area withthe highest concentration of Tree-of-Heaven.

Soyabean diseases

Soyabean diseases are major constraints to production in allsoyabean-producing regions of the world. The first SoybeanDisease Compendium [70] covered 50 diseases whereas thelatest edition lists more than 300 diseases [7]. The increasein the number of diseases and their expansion are a resultof the intense production and increased acreage in newregions of the world [8].Diseases tend to be geographically and environmentally

restricted [2]. Some diseases such as soyabean rust,Phakopsora pachyrhizi, are explosive by producing copiousamounts of spores and are widely distributed, whereas redleaf blotch, Phoma glycinicola, is restricted to a few countriesin Africa (Table 5). Diseases based on the season of thesoyabean crop consist of early-, mid- and late seasondiseases. Important and widely distributed early seasondiseases are bacterial pustule, Xanthomonas axonopodis pv.glycine, sclerotinia stem rot, Rhizoctonia solani, and seedlingblight and root and stem rot, Phytophthora sojae; diseasesattacking at mid-season are the Asian soyabean rust,P. pachyrhizi, and soybean mosaic virus; and late seasondiseases are charcoal rot, M. phaseolina, anthracnose/pod

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blight, Colletotrichum truncatum and the soybean cystnematode, H. glycines.The pathogens of soyabean diseases are bacteria, fungi,

oomycetes, viruses and nematodes (Tables 5–7). Thesepathogens cause visible disease symptoms on the entireplant, or on individual plant parts such as roots, stems,

leaves and pods. A diagnostic guide designed to providesoyabean growers, agronomists, pest management special-ists and others a means to diagnose soyabean diseases, asthey are observed in soyabean fields, has recently beenpublished [71]. The Field Guide to African SoyabeanDiseases and Pests, the first of its kind, highlights over

Table 5. Pests of soyabean and their geographical distribution: diseases bacteria and fungi

Diseases Asia Africa Europe N. America S. America Australia

BacteriaBacterial blightP. savastanoi pv. glycinea X X X X X XBacterial wiltCurtobacterium flaccumfacienspv. Flaccumfaciens

X X X X

Bacterial pustuleX. axonopodis pv. glycines X X X X X XWildfireP. syringae pv. tabaci X X X X X X

FungiBrown spotS. glycines X X X XCercospora leaf blightC. kikuchii X X X X X XCharcoal rotM. phaseolina X X X X X XDowny mildewPeronospora manshurica X X X X X XFrogeye leaf spotC. sojina X X X X X XRhizoctonia stem rotR. solani X X X X X XAsian soyabean rustP. pachyrhizi X X X X X XNew World soyabean rustP. meibomiae X XSclerotinia stem rotS. sclerotiorum X X X X X XTarget leaf spotC. cassiicola X X X XPod and stem blightD. phaseolorum var. sojae X X X X X XStem cankerDiaporthe var. meridionalis X X X XSouthern blightS. rolfsii X X X X XPowdery mildewMicrosphaera diffusa X X X X XAlternaria leaf spotAlternaria tenuissima X X XMyrothecium leaf spotMyrothecium roridum XAnthracnose/pod blightC. truncatum X X X X X XSudden death syndromeF. virguliforme(a.k.a. F. solani f. sp. glycines)

X

Sudden death syndromeF. tucumaniae XFusarium seedling/collar rotF. equiseti XRed leaf blotchP. glycinicola X

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20 diseases commonly found in many soyabean productionareas as well as those that may be unique to Africa. Theonline guide is available at: http://soybeaninnovationlab.illinois.edu/soybean-disease-diagnostic-guide.

BacteriaThree bacterial diseases – blight, pustule and wildfire –

attack soyabeans wherever they are grown (Table 5), if theweather conditions are favourable for their development.Severe infection by any one of the diseases may causepremature defoliation. In most years in Illinois, USA,bacterial blight and pustule can be found in 40–90% ofthe soyabean fields in the state [72]. The wildfire disease ismore serious in the southern United States. The prevalenceand the severity of these diseases fluctuate from year toyear, depending on weather conditions. Yield losses rangefrom zero to 15% with 1–2% common. Like many otherdiseases of soyabeans, bacterial diseases are more severe inwet years than in dry ones.Bacterial blight caused by Pseudomonas savastanoi pv.

glycinea is commonly found in cool, temperate soyabean-growing regions worldwide. Losses range from minimal to18% in Korea and the USA [73]. The disease has not caused

significant economic losses in most areas of the world dueto resistance (four genes identified) or plant tolerance. Inthe Philippines, infestation of plants with red spider mites(Tetranychus telarius) appeared to impart resistance orimmunity of soyabean to P. savastanoi pv. glycinea [73].This is the most common bacterial disease of soyabeans

in the major USA soyabean producing state of Illinois. Cool,rainy weather in June and July, accompanied by strongwinds, favours the development of bacterial blight. It ceasesto develop during hot, dry weather. Bacterial blight appearson soyabean leaves in June or early July as small, angular,yellow to light brown spots (lesions) with water-soakedcentres. As the tissues die, the centres of the lesions soonturn dark reddish brown to black and usually aresurrounded by a water-soaked margin bordered by ayellowish green halo. Infected young leaves frequently aredistorted, stunted and yellowish (chlorotic).Bacterial pustule is caused by the bacterium

X. axonopodis pv. glycines. In North America, this diseaseis typically present on the upper leaves. Initial infectionresults in the development of tiny pale green spots on thenew leaves. This disease can easily be confused withsoyabean rust. Mature soyabean rust pustules have a small

Table 6. Pests of soyabean and their geographical distribution: diseases – Oomycetes and viruses

Diseases Asia Africa Europe N. America S. America Australia

OomycetesPhytophthora rotP. megasperma X X X XPhytophthora seedling blight and root and stem rotP. sojae X X X X X X

VirusesCowpea mild mottle virusGenus Carlavirus X XBean pod mottle virusGenus Comovirus X X X XAlfalfa mosaic virusGenus Alfamovirus X X X X X XCucumber mosaic virusGenus Cucumovirus X X X X X XSouthern bean mosaic virusGenus Sobemovirus X X X X XSoybean mosaic virusGenus Potyvirus X X X X X XSoybean vein necrosis virusGenus Tospovirus XSoybean dwarf virus X X X XGenus LuteovirusTobacco ringspot virus X X X X XGenus NepovirusTobacco streak virus X X X X X XGenus IlarvirusPeanut stripe virus X X XGenus PotyvirusIndonesian soybean dwarf virus XGenus LuteovirusMungbean yellow mosaic virusGenus Geminivirus XSoybean crinkle leaf virusGenus Geminivirus X

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opening at the top for spore release whereas bacterialpustule lesions lack the opening on top and the spores [72].Like bacterial blight, Pseudomonas syringae pv. glycinea,

bacterial pustule over winters in crop residue and is carriedby wind or water droplets from the ground to the plant. Inaddition, the disease can be spread during cultivation whilethe foliage is wet. The bacterium will enter the plantthrough natural openings and wounds. Premature defolia-tion occurs due to heavy infections, which in turn producesa reduction in seed size and number.The symptoms of the pustule disease are somewhat

similar to those of bacterial blight. In bacterial pustule,

many small lesions may merge – producing large, irregular,mottled brown, dead areas with yellowish margins. Theleaves become ragged when parts of the brown, dead areastear away during windy, rainy weather. Severe infectionoften causes some defoliation.Wildfire: The name of the disease, wildfire, caused by

P. syringae pv. tabaci, results from the burnt appearance ofheavily infected tobacco plants. Wildfire disease rarelyoccurs in Illinois, USA but is most common in southernUSA [72].In 2006 and 2007, a new bacterial disease, wildfire, was

first observed in field-cultivated soyabeans in Mungyeong

Table 7. Pests of soyabean and their geographical distribution: diseases – nematodes

Diseases Asia Africa Europe N. America S. America Australia

NematodesPeanut podDitylenchus africanus XSoybean cystH. glycines X X X X XColumbia lance nematodeH. columbus X XPeanut root-knotM. arenaria X X X X X XRoot-knotM. ethiopica X X XRoot-knotM. hapla X X X X X XRoot-knotM. incognita X X X XRoot-knotM. javanica X X X X X XRoot-lesionP. brachyurus X X X X X XRoot-lesionP. crenatus X X X X X XRoot-lesionP. neglectus X XLesion nematodeP. scribneri XRoot-lesionP. teres XRoot-lesionP. thornei X X X X X XRoot-lesionP. zeae X X XReniformR. parvus X XReniformRotylenchulus reniformis X X X X X XReniformR. unisexus X XBritish spiralS. brachyurus X X X X X XSpiralS. truncatum XCommon spiral nematodeH. dihystera X X X X X XSpiralH. pseudorobustus X X X X X XStingB. longicaudatus X

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City, Korea. The disease caused severe blighting ofsoyabean leaves [74]. This disease is now widely distributed(Table 5).The symptoms of wildfire are light brown spots of

variable size and shape, which are surrounded by a broadyellow halo. The halo distinguishes wildfire from otherbacterial diseases of soyabean. In damp weather, the lesionsenlarge and merge forming large, dead areas in the leaf thatbecome dry, tear away, and produce tattered leaves. Abacterial pustule is almost invariably present in the centreof a wildfire lesion. Evidence exists that the presence ofbacterial pustule is required for wildfire infection. Bacterialblight lesions also may serve in the same way [72].

FungiMost of the soyabean fungal diseases occur in all sixgeographical regions (Table 5). A few such as sudden deathsyndrome, Fusarium virguliforme and F. tucumaniae, Fusariumseedling/collar rot, F. equiseti and red leaf blotch Phomaglycinicola only occur in North America, South America,Asia and Africa, respectively. The common names of thefungal pathogens are generally based on the plant partattacked and showing symptoms: root, collar, stem, leaf andpod. Common foliar diseases are frogeye leaf spot,Cercospora sojina, cercospora leaf blight, Cercospora kikuchii,target leaf spot, Corynespora cassiicola and soyabean rust,Phakopsora spp. Diseases attacking the stem are sclerotiniastem rot, Sclerotinia sclerotium and stem canker, Diaporthevar. meridionalis. Some diseases cause damage to severalplant parts such as pod and stem blight, Diaporthephaseolorum var. sojae. Sudden death syndrome, Fusariumspp., attack the roots but foliar symptoms typically appearat soyabean flowering. Soyabean anthracnose, caused by C.truncatum, produces brown, irregularly shaped spots onstem, pods and petioles [75]. In this section, we focus on afew economically important fungal pathogens.Rust: There are two closely related fungi that cause rust

on soyabean: P. pachyrhizi, sometimes referred to as theAsian or Australasian soyabean rust pathogen, but whichnow also occurs in the western hemisphere (Table 5) andP. meibomiae, the so-called New World soyabean rustpathogen, which is found only in the western hemisphere(Table 5). Except for a few minor characteristics, the twofungi appear morphologically identical, but P. pachyrhizi ismuch more aggressive on soyabean than P. meibomiae. Todate, P. meibomiae has not been documented to causesignificant yield losses in South America and has a restricteddistribution in North America [76].Asian soyabean rust, an invasive disease caused by

P. pachyrhizi, is a major disease limiting soyabean productionin many areas of the world [2, 77], and has been a seriousdisease in Asia for many decades [78]. It appeared in Africain 1997 and in the Americas in 2001. A hurricane, in 2004,probably brought it into the continental USA [79]. Before itwas first found in the continental USA, it was consideredsuch a threat that it was listed as a possible weapon ofbioterrorism [78]. Soybean rust cannot overwinter in areas

with freezing temperatures, but it can spread by windrapidly over such large distances, its development can be soexplosive, and it can cause such rapid loss of leaves, that it isnow one of the most feared diseases in the world’ssoyabean-growing areas [78].While soyabean rust usually begins in the lower canopy,

it quickly progresses up the plant until all of the leaves havesome level of disease. Severely diseased plants may becomecompletely defoliated. The loss of effective leaf tissueresults in yield reductions from both fewer and smallerseed. Yield losses as high as 80% have been reported [79]but the amount of loss depends on when the disease beginsand how rapidly it progresses. Besides leaves, soyabean rustcan also appear on petioles, stems, and even cotyledons,but most rust lesions occur on leaves [78].The first symptoms of soyabean rust, caused by

P. pachyrhizi, begin as very small brown or brick red spotson leaves. In the field, these spots usually begin in the lowercanopy at or after flowering. Lesions remain small (2–5 mmin diameter), but increase in number as the diseaseprogresses. Pustules, called uredines, form in theselesions, mostly on the lower leaf surface, and they canproduce many urediniospores. Soybean rust uredinios-pores are pale yellow-brown to colourless, with anechinulate (short spines) surface ornamentation. Thiscoloration is different from many other rust pathogenswhose spores are often reddish-brown (rust coloured).Germination of P. pachyrhizi urediniospores occurs throughan equatorial (central) pore, producing a germ tube thatends in an appressorium, which the fungus uses topenetrate the host directly or through a stoma. As moreand more lesions form on a leaflet, the affected area beginsto yellow, and eventually the leaflet falls from the plant [78].Red leaf blotch: There are only a few known

soyabean diseases that are not present in the majorsoyabean producing countries. Red leaf blotch, caused bythe pathogen Phoma glycinicola, formerly known asDactuliochaeta glycines [80], is one of them. Symptoms ofred leaf blotch include lesions on foliage, petioles, pods andstem [81]. Heavily diseased plants defoliate and senesceprematurely.Red leaf blotch is only known to occur in Africa (Table 5)

and was first reported from there in 1957 [82]. The diseaseis currently a threat to production in central and southernAfrican countries where it is endemic. P. glycinicola is asoil-borne fungus. It is known to infect soyabean andNeonotonia wightii, a perennial legume that inhabits thewoodlands and grasslands of southern Africa. The fungus isknown to occur in Cameroon, Ethiopia, Malawi, Nigeria,Republic of Congo, Rwanda, Uganda, Zambia andZimbabwe. Most of the published literature about red leafblotch is from studies completed in Zambia and Zimbabwe,where yield losses of up to 50% were reported [83].Because the fungus does not produce copious spores like

P. pachyrhizi, is not seed-borne, and trade of soyabeans outof Africa is limited, the pathogen has not spread to newlocations. However, it is a serious, potentially invasive pest.

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It is predicted that the pathogen would most likely survivethe non-crop season in any of the yet unaffected soyabeanproduction regions worldwide [2]. If the fungus/disease isfound in the USA, it may become economically important,because of its potential to cause significant yield losses, thelack of resistant soyabean varieties, and the importance ofthe soyabean crop to the agro-industry in the USA [84].

OomycetesOomycetes are fungal-like microbes that cause highlydestructive plant diseases that affect agriculture, horticul-ture and forestry. Oomycetes occupy both saprophytic andpathogenic lifestyles, and include some of the mostnotorious pathogens of plants. Soyabean is a high-valuecrop that is heavily impacted by oomycete diseases. Thereare many oomycete species attacking soyabean with themore important species belonging to the Pythium andPhytophthora genera. Among the oomycetes, the mostaggressive plant pathogenic species are found in thePhytophthora genera. Phytophthora rot, Phytophthora mega-sperma and phytophthora root and stem rot, P. sojae areimportant and widely distributed diseases (Table 6).Phytophthora sojae: This disease, prevalent in many

soyabean production regions of the world, is an Oomycetethat causes a serious root and stem rot of soyabeans. Thepathogen can survive for long periods in infected planttissue or soil as sexual spores called oospores [85]. It cankill and damage seedlings and plants throughout thegrowing season from the time of planting nearly untilharvest. This disease is favoured by wet and warm soilconditions, especially saturated conditions early in thegrowing season. In the early season, seedlings can beattacked and killed in the ground or soon after emergence.At seedling and later vegetative stages, infected stemsappear bruised and are soft, secondary roots are rotted, theleaves turn yellow, and brown and plants can wilt and die.During mid or late season, plants may die throughout

the season. On infected plants, brown lesions form onthe roots, the roots rot and degrade, and a darkchocolate-brown discoloration of the stem often extendsfrom below the soil line upwards into lower parts of theplant. Leaves turn yellow, wilt and typically, stay attachedafter plant death. Plants are often killed in patches or insections of rows [86]. Over the last 11 years, Phytophthorahas suppressed US soyabean yields resulting in an estimated500 million-bushel loss. Today, P. sojae remains a top threatfor growers to manage worldwide and is the no. 1 diseasethat impacts soyabean yields [87].

VirusesA number of viruses affect soyabean production on anannual basis (Table 6). Although yield loss from viruses isgenerally relatively low, individual fields may suffer fromsignificant losses in any given year. Viruses are infectioussubmicroscopic particles made up of DNA or RNAenclosed by a protein coat. Soyabean viruses are generallytransmitted by insect vectors such as aphids, beetles and

whiteflies although Tobacco ringspot virus is also trans-mitted by the dagger nematode [88] (https://soybeans.ces.ncsu.edu/depts/pp/notes/Soybean/soy009/soy009.htm).Depending on the genotype and age of infection,

symptoms range from mosaic and mottling, leaf curling,green vein banding and stunting. Most severe symptoms areobserved on plants infected at early growth stages.Soyabean viruses with a worldwide distribution include

the Alfalfa mosaic virus (AMV, Alfamovirus); Cucumbermosaic virus (CMV, Cucumovirus); Soybean mosaic virus(SMV, Potyvirus); Tobacco streak virus (TSV, Ilarvirus) andSoybean yellow mosaic virus (SYMV, Potyvirus) (Table 6).Viruses restricted to Asia are the Indonesian soybean dwarfvirus (ISDV, Luteovirus); mungbean yellow mosaic virus (MYMV,Geminivirus) and the soybean crinkle leaf virus (SCLV,Geminivirus).About 50 viruses have been reported to occur in

soyabean in various parts of the world. Of these,13 viruses have been reported from Southeast Asiancountries. These viruses cause economic yield losses, andare sometimes a major limiting factor in soyabeanproduction [89]. The most important soyabean viruses inSoutheast Asia are Soybean mosaic potyvirus (SMV), Peanutstripe potyvirus (PStV), Cowpea mild mottle Carlavirus(CMMV), Mosaic Cucumovirus, Soybean Stunt Strain(CMV-SS), Indonesian soybean dwarf Luteovirus (ISDV),Mungbean yellow mosaic Geminivirus (MYMV), Soybeancrinkle leaf Geminivirus (SCLV) and Soybean yellow mosaicvirus (SYM). SMV, considered the most common virus foundin soyabean throughout the world, is found in everySoutheast Asian country where soyabean is grown. PStV isalso widely distributed, since this virus is common in peanutplants throughout the region. Of the 13 soyabean virusesfound in Southeast Asia, six are seed-borne and five aretransmitted by vectors in a persistent manner [89].Three most common soyabean virus diseases in

northern Nigeria are the mosaic diseases, cowpea mildmottle virus (CPMMV, Carlavirus), transmitted by thewhitefly, B. tabaci; bean pod mottle virus (BPMV, Comovirus);alfalfa mosaic virus (AMV, Alfamovirus); cucumber mosaic virus(CMV, Cucumovirus) and the southern bean mosaic virus(SBMV, Sobemovirus) [90].The BPMV and SMV are the most common viruses

infecting soyabean in North Carolina, USA [88]. Symptomsof the two most common viruses, BPMV and SMV mayoverlap and soyabean plants may be infected with bothviruses. Tests to accurately identify each virus are available,but are rarely used, because taking corrective action israrely possible. Tobacco ringspot virus (TRSV) is commonin North Carolina but yield losses in production fields aregenerally insignificant.Bean pod mottle virus: BPMV, though generally less

common than SMV can severely lower soyabean yield ininfected fields. BPMV causes mottling of the leaves, leafdistortion, stunting of the plant, and mottled seed. BPMVhas also been implicated in the ‘green stem syndrome’ andthis can result in additional yield losses. Green stem

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syndrome is the condition where the stems of matureplants remain green and leathery making harvest difficult.The severity of symptoms is related to the virus strain,soyabean variety and how early the plant is infected. Yieldloss to BPMV is generally related to time of infection; earlyinfection can result in severe losses. Virus transmissionthrough seed is very low, generally <0.01%. Like SMV, hightemperatures limit BPMV symptom expression, whereascool temperatures enhance development of leaf symptoms.BPMV is transmitted by several species of leaf feedingbeetles, including bean leaf beetle, Ceratoma trifurcata.Overwintering beetles probably acquire virus from wildlegume weed species. The incidence of BPMV infectionin soyabean fields can be very high in years whenoverwintering bean leaf beetle populations are high [88].Soybean mosaic virus: SMV may be seed-borne or

transmitted by aphids including the soybean aphid, Aphisglycines. SMV causes raised areas or puckering on the leafsurface, stunting of the plant and mottling of the seed. Seedmottling, however, may be caused by other factors. Theprimary leaves of plants grown from infected seed mayshow mottling and downwards curling. Infected plants areusually stunted because of shortening of the petioles andinternodes, particularly when infected while still young orwhen infected from the seed. Some cultivars developprogressive necrosis of the petioles and stems, budnecrosis, defoliation and plant death with some strainsresembling the bud blight of soyabean caused by Tobaccoringspot virus and Tobacco streak virus [91].The pods are reduced in number and size, some are

malformed, glabrous or seedless, and the yield may beconsiderably reduced. The virus can reduce the size of theseed, particularly in the case of co-infection with BPMV,change its chemical composition, diminish seed viability,seed germination and seedling vigour and thus the quality ofthe seed [92].The severity of symptoms is related to the virus strain,

soyabean variety and the age of the plant when it is infected.Symptom expression is also influenced by temperature.High temperatures limit symptom expression, whereascool temperatures enhance development of leaf symptoms.Frequently, the crop may appear healthy until several daysof cool weather in late summer or early autumn, when theentire crop appears to be affected [88].Yield loss to SMV is generally related to time of infection.

Virus transmission through seed may be as high as 30%.When infected seed is planted aphids may spread thedisease from infected plants to the remainder of thesoyabean crop. Wild hosts of SMV are relatively rare [88].The incidence of SMV infection in USA soyabean fields

has been much lower than that reported for BPMV.However, yield losses from SMV infection in the NorthCentral Region have been as high as 94%. When soyabeanplants are infected with both BPMV and SMV, symptoms canbe more severe than infection by either virus alone [93].Tobacco ringspot virus: TRSV is found in all regions

except in Europe (Table 6). Principal symptoms of TRV

include stunting, leaf distortion and characteristic browningand curling of the terminal branch. The most obvioussymptoms are the proliferation of buds and flowers, andlack of pods or poorly formed pods. Stems remain greenand petioles may remain attached with black lesions. Thestems remain green because the plants are sterile as a resultof pod abortion. Infected plants will stand out in a maturesoyabean field because of the green stems. If there are largenumbers of these green plants, harvest may be difficult. Theprimary impact of this disease is that soyabean grown forseed from fields with this virus cannot be shipped to certaincountries.Although the virus may be seed-borne, this is probably

not an important means of transmission since most infectedplants are sterile. The dagger nematode can transmit thisvirus, but the virus does not move from the roots to theshoots and leaves of the soyabean plant [88]. Spread isprobably by thrips and aphids, though no efficient vectorhas been identified [93].Tobacco streak virus: TSV has a worldwide distribution

(Table 6) and a wide range of hosts [93, 94]. Plants ofMelilotus albus (honey clover), a biennial legume, are theprimary reservoir of TSV in the northwest USA [95].Tobacco streak virus is transmitted by thrips, and throughinfected soyabean seed. TSV infection can be difficult todetect because the concentration of TSV particles declinesignificantly as soyabean plants mature [93].TSV is prevalent in southeastern Brazil, and can limit

yields of soyabeans in some years [96]. Epidemics ofsoyabean bud blight, caused by TSV, were monitored intwo soyabean cultivars sown on seven different dates in1987–88 in Arapoti County, Parana. The highest final levelof disease incidence was 60% in 1987 and 90% in 1988 [97].Brazilian bud blight is also a serious disease in the Santa FeProvince of Argentina [98]. It occurs in the USA [95, 99]but is of no economic significance on soyabeans becauseconditions are not conducive to disease development.

NematodesPlant-parasitic nematodes are recognized as one of thegreatest threats to crops throughout the world. There aremany nematode genera and species attacking soyabeansworldwide (Table 7).As of 2015, 18 plant-parasitic nematode genera and

48 species have been associated with soyabean in SouthAfrica alone [100]. Globally, the economically mostimportant genera consist of Ditylenchus (peanut pod),Heterodera (cyst), Hoplolaimus (lance), Meloidogyne(root-knot), Pratylenchus (root-lesion), Rotylenchulus(reniform), Scutellonema (spiral), Helicotylenchus (spiral)and Belonolaimus (sting) (Table 7).The root-knot nematodes, Meloidogyne arenaria,

M. hapla and M. javanica; root-lesion nematodes (RLN),Pratylenchus brachyurus, P. crenatus and P. thornei;reniform nematode, R. reniformis; British spiral nematodeScutellonema brachyurus; common spiral nematode,Helicotylenchus dihystera; and the spiral nematode

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H. pseudorobustus are present in all global regions (Table 7).The SCN, H. glycines is present in all regions except inAustralia. The peanut pod nematode, D. angustus, occursonly in Africa, lesion nematode P. scribneri in NorthAmerica, spiral nematode S. truncatum in Africa and thesting nematode B. longicaudatus in North America (Table 7).Plant-parasitic nematodes are among the most serious

disease problems in soyabean production. Disease causedby nematodes results in an estimated annual loss of 3–4% insoyabean yield the USA. A number of physical andbiological factors influence the extent of damage causedby nematodes. Plant growth and yield are directly related tothe numbers of plant-parasitic nematodes in the soil atplanting (preplant population density). Most methods formanaging these parasites involve lowering their initialnumbers to levels at which plant damage is minimized.Soil type and texture have a marked influence on thedamage caused by these organisms. Sandy soils favour mostspecies of plant-parasitic nematodes. Since sandier fieldshave poor soil moisture-holding capacities and limitednutrient reserves, damage in these soils may be moresevere. Soil pH and fertility problems as well as a hard pantend to enhance damage caused by parasitic nematodes.Alleviating these problems will not eliminate nematodeproblems, but may be helpful [101].SCN H. glycines: The SCN occurs in most soyabean

growing regions [7] (Table 7). The nematode presents athreat to all regions of the world where soyabeans aregrown and steps should be taken to prevent introduction inthe first instance and to control spread once the nematodeis known to be present [102]. The nematode is spread mosteasily via infested soil and contaminated machinery. Anymechanism that spreads infested soil can be a means ofdispersal, including wind, water, migratory birds and seedlots [103].H. glycines attacks a wide range of Fabaceae. Members of

Caryophyllaceae and Scrophulariaceae are also hosts. Riggsand Wrather [104] provide a list of non-fabaceous hostscomprising 63 species in 50 genera from 22 families.Symptoms on the root system range from slight

discoloration to severe necrosis [2]. Diagnosis is confirmedwhen white or yellow females are observed attached toroots. Above ground symptoms, often not readily apparent,include slight to severe plant stunting and leaf chlorosis.Symptoms may be enhanced or repressed in associationwith other pathogens [105].It is the most important soyabean disease in the USA

[106]. It is particularly important in the semi-arid areas.Soyabean disease loss estimates were compiled for the1994-harvested crop from the ten countries with thegreatest soyabean production (Argentina, Bolivia, Brazil,Canada, China, India, Indonesia, Italy, Paraguay and theUSA). The objective was to document the major soyabeandisease problems in these countries and any recent changesin the severity of individual soyabean diseases. Total yieldlosses caused by H. glycines, in these ten countries, weregreater than those caused by any other disease [107].

Roots infected with SCN usually have reducedRhizobium nodulation and are short, sparse and dark incolour. With careful examination, small period-sizeddot-like cysts on the roots can be seen. These are thedeveloping females of the SCN and can range in colourfrom white to creamy yellow to dark brown [108].Reported yield losses on soyabean vary from 10 to 70%

in Japan [109, 110]. All soyabean growing areas in the USAare at risk. Losses in the southeastern USA were estimatedat US$88.4 million in 1990 [111]. Wrather et al. [106]reported on losses due to H. glycines and other diseases onsoyabean in the USA. The reduction in yield in 2002amounted to US$784 million and yield losses wereestimated at 3.6 million tonnes in 2001.Columbia lance nematode: Hoplolaimus columbus

has been reported from several different countries aroundthe world, including infestations in India, Pakistan, Egypt andthe United States [112]. In the USA, H. columbus is limitedmainly to the southeastern part of the country. In sandyloam soils, on favourable hosts, it often replacesMeloidogyne incognita as the predominant species [113].Maize, cotton and soyabean are good hosts for thisnematode.The Columbia lance nematode feeds both externally and

internally on soyabean roots. Lesions may develop on theroots that can coalesce and give the appearance of a rootrot [114]. Symptoms of feeding are taproot stunting,increased secondary branching, above ground stunting,wilting and mild chlorosis. Infected soyabeans bear only afew pods [113].This nematode remains wormlike throughout its life

cycle and can only be identified microscopically. Thepopulation densities of this nematode fluctuate only slightlyduring the course of a year. The amount of damage tosoyabean and subsequent yield loss will be directlyproportional to the density of this nematode at soyabeanplanting. Nematode densities are generally in themoderate-to-high range following these crops [114].Root-knot nematodes, Meloidogyne spp.: Five root

knot nematodes are of major importance; M. arenaria,M. ethiopica, M. hapla, M. incognita and M. javanica.Root-knot nematodes are generally the predominantplant parasitic nematodes associated with soyabean cropsin South Africa [115, 116] and are considered as a seriousconstraint to production of the crop worldwide [117, 118].Distinct root galling, caused by the feeding of female

root-knot nematodes, represent below ground symptoms.Above ground symptoms, in fields where high populationlevels of root-knot nematodes occur, can include stuntedplants and leaf yellowing [100].M. incognita and M. javanica are the predominant

nematode pests in South Africa [100] and are of majorimportance worldwide.M. incognita is predominantly foundin warmer climates, at latitudes between 35°S and 35°N[119]. It is a damaging pathogen of soyabean and othercrops throughout the southern United States [120]. In the1970s, soyabean yield reductions reached as high as 90% for

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susceptible soyabean cultivars in the presence ofM. incognita in some areas [121]. The impact ofM. incognita on soyabean production has been reducedwith the availability of resistant cultivars. However, annualsoyabean yield losses to this nematode during 1999–2002still exceeded 99.6 thousand metric tonnes in theUSA [106].RLNs, Pratylenchus spp.: Several species of RLNs may

affect soyabeans globally (Table 7). However, the principalspecies are P. brachyurus and P. crenatus, which occur in allregions; P. scribneri which only occurs in North America;P. teres, a pest limited to Africa and P. thornei and P. zeaewhich occur in Africa, North America and Australia.P. brachyurus has more than 80 hosts worldwide [122].

P. brachyurus is the principal soybean nematode inSoutheastern USA. This nematode, like Columbia lancenematode, remains wormlike throughout its life cycle.Lesion nematodes penetrate soyabean roots, feed internallyon the root, and lay eggs within the root system [101]. Thesymptoms caused by this parasite are non-specific. Damagesymptoms are reduced root systems with necrotic streaksor lesions. The lesions on roots may coalesce to give theappearance of a root-rot [101]. Leaves wilt and haveabnormal colours, stems show rosetting and seeds havelesions. Severe damage kills entire plants [122].Damage to soyabean caused by this pathogen is usually

restricted to sandy loam and sandy soils in the southeasterncoastal plain of North Carolina. Delaying soyabean plantinguntil mid-June, as done with double-crop wheat/soyabeansystems or rotation with maize, frequently can be used tomanage this nematode. Tobacco and peanuts should not beused in rotation with soyabean if lesion nematode is aproblem. While these crops are poor hosts for lesionnematode, they may be damaged by the high numbers thatbuild up on soyabean [101].Pratylenchus thornei is one of the most widely distributed

species of Pratylenchus and has been reported from everycontinent except from Antarctica [123]. A major host iswheat but it has about 40 other hosts including soyabean[122]. Of the 22 predominant nematode species recoveredfrom soyabean soil in South Africa, P. thornei ranks 9th inmean population density compared with the most abundantspecies P. zeae [116].It is an obligate migratory endoparasite that first feeds

externally then enters plant roots, feeds, reproduces andmoves freely within the tissue while spending its entire lifecycle there. The species can also be found in soil aroundroots. Within the roots, feeding is confined to the rootcortex. Like other Pratylenchus species, P. thornei has six lifestages: egg, four juvenile stages and adults. Reproduction isby parthenogenesis [124].In general, root lesion infection results in plants

exhibiting symptoms of chlorosis, wilting and stunting.Infected roots show initial symptoms of small, water-soaked lesions that soon turn brown to black. Lesions areformed along the root axis and may coalesce laterally togirdle the roots that are killed. Affected root tissue may

slough off leaving a severely reduced root system.Secondary infection by fungi and bacteria may furtherdestroy the root system by causing the sloughing off theroot tissues and rot. Plant yield is reduced and in severeinfections, plants may be killed [124].Reniform nematodes Rotylenchulus spp.: Reniform

nematodes in the genus Rotylenchulus are semi-end parasitic(partially inside roots) species in which the femalespenetrate the root cortex, establish a permanent-feedingsite in the stele region of the root and become sedentary orimmobile. The anterior portion (head region) of the bodyremains embedded in the root whereas the posteriorportion (tail region) protrudes from the root surface andswells during maturation. The term ‘reform’ refers to thekidney shaped body of the mature female [125].Rotylenchulus reniformis is largely distributed (Table 7) in

tropical, subtropical and warm temperate zones in SouthAmerica, North America, the Caribbean Basin, Africa,southern Europe, the Middle East, Asia, Australia and thePacific [126]. It was first found on cowpea roots inHawaii [127].At least 314 plant species can act as hosts to reniform

nematodes. Among them, cotton, cowpea, soyabean,pineapple, fruit crops, tobacco tea and various vegetablesare the most common hosts [101]. Robinson et al.published a list of hosts and nonhosts for the reniformnematode [128].Only females infect plant roots. After infection, a feeding

site composed of syncytial cells is formed. A syncytial cell isa multinucleated cell resulting from cell wall dissolution ofseveral surrounding cells.R. reniformis has a life cycle similar to those of root knot

and cyst, but signs or symptoms for the reniform nematodeare not readily visible to the naked eye. The amount andtype of damage incurred often depends on the host speciesand/or cultivar as well as the nematode population. Generalsymptoms include reduced root systems, leaf chlorosis,overall stunting of host plants, and reduced yields and plantlongevity [125].Sting nematode, Belonolaimus longicaudatus: Sting

nematodes are endemic to the southeastern United States(Table 7) and are only capable of reproducing in sandy soils.This fact is the primary limiting factor in this nematodesdistribution. It is an extremely damaging nematode tocotton, maize, peanut and soyabean [101]. This pathogen isalways wormlike and microscopic. The sting nematode is anectoparasite that feeds externally on the root and lays itseggs in the soil.Sting nematodes do not enter plant roots to feed. They

inject a toxic enzyme into the roots of their host whilefeeding, resulting in significant damage, yield loss and evenplant death [129]. Symptoms of sting nematode damage arepoor growth and short roots with many rootlets at theends of the roots. Roots may have a ‘stubby’ appearance.Plants that escape damage from this nematode early in theseason may have a taproot with a few lateral roots, but nofibrous root system. Fortunately, the occurrence of this

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nematode is limited to very sandy soils. Fields infested withthis nematode should be considered for uses other thanrow crops. Watermelon and tobacco will not supportreproduction of this nematode and can be used in rotationwith soyabean where this nematode is a problem [101].

Weeds

There are numerous weed species that are important bioticconstraints in soyabean production worldwide of which thekey species are listed in Table 8. The weed species are notspecific to soyabeans and species composition depends onthe locally occurring species, which are general pests ofmost local crops.Heavy weed infestations in soyabeans greatly interfere

with the timeliness and efficiency of harvests, and if notcontrolled, cause severe losses in crop production. Lossescan reach 100% depending on the soil preparation, status ofthe crop, weed species present and environmental factors.Studies in India indicated a 42% loss in soyabean yield whencomparing yields in weedy check plots compared withweed free plots. Net returns, due to weed infestation, werereduced by 53% [130].Perennial and most annual weeds are a problem in

soyabean in the early growth stages. Because soyabeans areweak competitors in the early part of the crop season,weeds outgrow them. Soyabeans usually develop a fullcanopy by 8 weeks after emergence and can then competeeffectively with weeds up to maturity. Little or no reductionin yield occurs if soyabean is kept weed free for the first 4weeks after plant emergence. This is the critical period forweed competition in soyabeans [131]. Therefore, weedcontrol at an appropriate time, using a suitable weedcontrol method, is a requirement to ensure effectiveweed management and high grain yields in soyabean.Morphologically weeds are classified as Monocotyledons

(grasses and sedges) and Dicotyledons (broad-leaved). Thetop ten worst weeds in corn (maize) and soyabeans assummarized by US university scientists [132] list eightbroad-leaved weeds and two grassy weeds. Broad-leavedweeds are: velvetleaf, Abutilon theophrasti; common water-hemp, Amaranthus tuberculatus and Palmer amaranth,A. palmeri; giant ragweed, Ambrosia trifida; commonlambsquarters, Chenopodium album; horseweed/marestail,Conyza canadensis; bur cucumber, Sicyos angulatus andthree-lobe morning glory, Ipomoea triloba. The two grassyweeds listed among the top ten worst weeds are: woollycupgrass, Eriochloa villosa and giant foxtail, Setaria faberi(Table 8).Broad-leaved weeds that have a worldwide distribution

are slender amaranth, A. viridis; common lambsquarters,C. album; horseweed/marestail, C. canadensis and wildpoinsettia, Euphorbia heterophylla. Grassy weeds that arepresent in all global regions are crowfoot grass,Dactyloctenium aegyptium; goose grass, Eleusine indica;

yellow foxtail, Setaria pumila and green foxtail, S. pumila(Table 8).

Invasive weedsSome of the most serious weeds in soyabeans are referredto an ‘invasive’ or ‘alien’ species. Due to the disturbance ofthe soil in soyabean crop production, many areas areinfested with invasive weed species. The term ‘invasive’ asmost often used applies to introduced species (also called‘non-indigenous’ or ‘non-native’) that adversely affect thehabitats and bioregions they invade economically, environ-mentally or ecologically.Common invasive species traits include the following:

fast growth, rapid reproduction, high dispersal ability,phenotypic plasticity (the ability to alter growth form tosuit current conditions), tolerance of a wide range ofenvironmental conditions (ecological competence), ability tolive off of a wide range of food types (generalist), associationwith humans [133] and prior successful invasions [134].Among the broad-leaved species, that are severe invasive

weeds, are the pigweeds (Amaranthaceae), commonwaterhemp, A. tuberculatus; slender amaranth, A. viridis;and Palmer amaranth, A. palmeri. Serious invasive grassyweed species include the foxtail (Poaceae) species, giantfoxtail, S. faberi; yellow foxtail, S. pumila and green foxtail,S. viridis (Table 8).

PigweedsAmaranthus, collectively known as amaranth [135], is acosmopolitan genus of annual or short-lived perennialplants. Some amaranth species are cultivated as leafyvegetables, pseudocereals and ornamental plants. Most ofthe Amaranthus species are summer annual weeds and arecommonly referred to as pigweed.Pigweed is the common name for several closely related

summer annuals that have become major weeds ofvegetable and row crops throughout the United Statesand much of the world [136]. Most pigweeds are tall,erect-to-bushy plants with simple, oval- to diamond-shaped, alternate leaves and dense inflorescences (flowerclusters) comprised of many small, greenish flowers.Pigweeds thrive in hot weather, tolerate drought,

respond to high levels of available nutrients and areadapted to avoid shading through rapid stem elongation.They compete aggressively against warm season crops, andreproduce by prolific seed production.Also called amaranths, pigweeds are native to parts of

North and Central America. Crop cultivation and humancommerce have opened new niches, allowing pigweeds toinvade agricultural ecosystems throughout the Americas,and parts of Europe, Asia, Africa and Australia (Table 8).Most amaranths make nutritious green vegetables or graincrops, and deliberate planting for food has helped someweedy species spread around the world [136].Pigweeds are highly responsive to nutrients, especially

the nitrate form of nitrogen (N) [137]. Fertilizationenhances both weed biomass and seed production.

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Pigweeds in soyabeans are reported to host pestnematodes (Meloidogyne spp.) and many crop pathogens,including fungi that cause white mould (S. sclerotiorum) andsouthern blight (Sclerotium rolfsii) [137].The pigweeds, common waterhemp A. tuberculatus, and

slender amaranth and Palmer amaranth, A. viridis andA. palmeri, are included in the list of the top ten worstweeds in maize and soyabeans [132]. Common waterhempis restricted to West Asia, Europe and North America[138] while slender amaranth [139] and Palmer amaranthoccur worldwide (Table 8).A. tuberculatus is an annual dioecious herb, 1–2 m tall,

which has spread from its native range in northern NorthAmerica and is considered a major weed of agriculturalfields and other disturbed areas in 40 US states. In themid-western USA, it has become increasingly difficult tocontrol over the past 10 years due to a persistent seedbankand the development of resistance to certain herbicides.

A. tuberculatus seed is a known contaminant of soyabeanseed and other grains, and has been accidentally introducedand become naturalized in parts of West Asia and Europe.Potential spread to other areas is considered likely.A distinguishing characteristic of A. tuberculatus that sets

it apart from similar members of the genus Amaranthus isthe lack of hair on its stems and leaves. This characteristicgives the plant a bright, glossy appearance Amaranthus viridis,an annual herb, which grows from 6 to 100 cm high [139],is native to the southern United States and Mexico [140].It is one of the most common weeds in the tropics,subtropics and warm temperate regions. A. viridis occursvirtually in all disturbed habitats and all crops, herbaceousand woody, in all but the wettest soils throughout thewarmer regions of the world. Other Amaranthus speciesmay be confused with this plant but A. viridis can bedistinguished by its wrinkled fruit and its flower bracts being<1 mm long and acute (pointed).

Table 8. Pests of soyabean and their geographical distribution: weeds

Weeds Asia Africa Europe N. America S. America Australia

Broad-leaved weedsVelvetleaf X X X XA. theophrastiCommon waterhempA. tuberculatus XSlender amaranthA. viridis X X X X X XPalmer amaranthA. palmeri X X XGiant ragweedA. trifida X X XCommon lambsquartersC. album X X X X X XHorseweed/marestailC. canadensis X X X X X XBurcucumberS. angulatus X X XThree-lobe morning gloryI. triloba X X X X XAsian spider flowerCleome viscosa XWild poinsettiaE. heterophylla X X X X X XCommon sunflowerHelianthus annuus X

Grassy weedsCrowfoot grassD. aegyptium X X X X X XGoose grassE. indica X X X X X XWoolly cupgrassE. villosa X XGiant foxtailS. faberi X XYellow foxtailS. pumila X X X X X XGreen foxtailS. viridis X X X X X XHorse purslaneTrianthema portulacastrum X

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A. viridis is used as a traditional medicine in NorthAmerica. It is eaten in the northeastern Indian stateManipur where it is known as Cheng-kruk and eatentraditionally as a vegetable in South India, especially inKerala, where it is known as ‘Kuppacheera’. It is also eatenas a vegetable in parts of Africa [141]. In Jamaica it is eatenas a vegetable and is known locally as ‘callaloo’. Its use as afood may be the reason that this invasive weed has spreadglobally.Amaranthus palmeri is a species of edible flowering

plant in the amaranth genus. It has several common names,including carelessweed, dioecious amaranth, Palmer’samaranth, Palmer amaranth and Palmer’s pigweed. Theleaves, stems and seeds of Palmer amaranth, like those ofother amaranths, are edible and highly nutritious. Palmeramaranth was once widely cultivated and eaten by NativeAmericans across North America, both for its abundantseeds and as a cooked or dried green vegetable. It is nativeto most of the southern half of North America. Populationsin the eastern United States are probably naturalized.It has also been introduced to Europe, Australia and otherareas [142].Palmer amaranth is the most competitive and aggressive

pigweed species. Season-long competition by Palmeramaranth at 2.5 plants per foot of row can reduce soyabeanyield by as much as 79% [143]. In Kansas, USA soyabeanyield reduction of about 78% was reported by Palmeramaranth, at a density of 8 plants/m2. Early emerging Palmeramaranth plants also cause more soyabean grain yield losswhen compared with later-emerging plants [144]. Palmeramaranth, referred to as a ‘superweed,’ is considered athreat most specifically to the production of geneticallymodified (GM) cotton and soyabean crops in the southernUnited States, because it has developed resistance toglyphosate. It has also been referred to as ‘a weed strongenough to stop combines’ [145].Palmer amaranth emerges later than many summer-

annual weeds and continues to emerge throughout thegrowing season. This extended emergence pattern makes itdifficult for preemergence and nonresidual postemergenceherbicides to control later-emerging plants.The widespread adoption of no-tillage systems, reduced

reliance on soil-applied residual herbicides, and increasedherbicide resistance have contributed towards theincreased infestation of Palmer amaranth in differentcropping systems [146].The high relative growth rate of Palmer amaranth makes

control with postemergence herbicides difficult. In thesouthern United States, Palmer amaranth has been docu-mented to grow as much as 2.5 inches per day [143]. Unlikeother pests, it can continue to grow an inch a day evenwithout water, making it particularly adept during drought.It also thrives in hot weather, continuing to grow whentemperatures top 90 °F and other plants shut down [147].Each female plant produces as many as 500 000 seedlings,

meaning just one plant can birth an entire field [147]. It canhybridize with other pigweeds. Its dioecious reproduction

(separate male and female plants) forces outcrossing andgenetic diversity that allows it to readily adapt to newenvironmental conditions and quickly spread herbicideresistance genes when selection pressure is applied [148].

FoxtailsThe foxtails, members of the Setaria genus, are one of theworst weed groups interfering with North American andworld agriculture and land management [149, 150]. Theinflorescence resembles a foxtail, hence the common name.The weedy Setaria spp., S. faberii (giant foxtail), S. pumila(yellow foxtail) and S. viridis (green foxtail) [151, 152] areconsidered among the top ten worst weeds [132].Five successive waves of Setaria spp. invasion from

pre-agricultural times to the present have resulted inwidespread infestation of the disturbed, arable, temperateregions of the earth. These invasions have resulted inconsiderable economic and environmental costs [132]. Theorigin of the genus and the original wild Eurasian Setaria sp.was probably Africa, based on the large number of Setariaspp. from there (74 of 125), as well as genomic evidence oftropical origins [152, 153].The success of the Setaria spp.-group is due to their

intimate evolutionary relationship with humans, disturb-ance, agriculture and land management. Genotypic andphenotypic biodiversity provide this species-group withtraits that allow them to invade, colonize, adapt to andendure in a wide range of disturbed habitats in temperate,tropical and sub-tropical regions [154].S. faberi, giant foxtail, also referred to as Japanese

bristlegrass, is an annual grass, reproducing by seeds. It canreach 0.61–1.5 m in height. Leaves are up to 41 cm long,15–25 mm wide. The leaf blade has short hairs that coverthe upper surface. The ligule has a fringe of hairs [155].Flowering occurs in late summer to early autumn, when agreen (eventually straw-coloured), bristly inflorescencedevelops.S. faberi, a native of Asia, was accidentally introduced into

the United States in the 1920s as a contaminant of othergrain [155]. It is also present in some European countries[156]. Plants invade disturbed sites such as fields, roadsides,landfills, fencerows and right of ways.Giant foxtail is one of the most prevalent annual grasses

infesting crop production fields in the Midwest, USA [157].This is partially due to its prolific production of seed andtheir subsequent longevity in the soil. Giant foxtailinterferes with soyabean growth and reduces yield. In a3-year study, an infestation of 54 plants per 0.3 m rowreduced soyabean seed yield 28%. In addition, the increasein giant foxtail dry matter with increasing weed density wasproportional to the decrease in dry matter of thesoyabeans.S. pumila, yellow foxtail, is a cosmopolitan species that

occurs in all regions (Table 8). Soyabeans are among themany hosts worldwide [158]. S. pumila is a tufted annualgrass, very variable in size and vigour ranging from a fewcentimetres up to more than 100 cm high. It is much

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branched and there may be rooting at lower nodes. Thestem base and lower leaves are often red or purplish,especially under infertile soil conditions. The leaves aregenerally glaucous (‘gleaming’, the meaning of ‘pumila’),up to 30 cm long by 1 cm wide, and glabrous except for afew long hairs on the upper surface near the base [158].S. pumila can act as an alternative host of Claviceps

purpurea (ergot), Pythium graminicola (root rot), Sclerosporagraminicola (downy mildew), Ustilago neglecta (smut),Anoecia corni (dogwood aphid), Rhopalosiphum maidis(green corn aphid), Pyricularia grisea (rice blast), Cirphiscompta (paddy cutworm) and Diabrotica longicornis (north-ern corn rootworm).Setaria viridis, a species of grass known by many

common names, including green foxtail, occurs in allworld regions [159] (Table 8). It is sometimes considereda subspecies of Setaria italica. It is native to Eurasia, but it isknown on most continents as an introduced species and isclosely related to S. faberi, a noxious weed. A hardy grass,it grows in many types of urban, cultivated and disturbedhabitats. It is the wild antecedent of the crop foxtailmillet [160].S. viridis is a native of Europe but spread to North

America as early as 1821 [161] and now occurs in mosttemperate countries of the Northern and Southern hemi-spheres. It rarely occurs in the tropics other than at highaltitudes.

Management of Soyabean Pests

A detailed package of practices for managing soyabeanpests, diseases and weeds has been developed in India[162]. The management practices are based on crop stages:period between crops, pre-sowing, sowing, vegetativestage, reproductive stage and harvest (Table 9). At eachcrop growth stage, the major pest management practicesemployed consist of (1) mechanical methods; (2) culturalcontrols; (3) host plant resistance; (4) biological controlagents (parasitoids, predators and pathogens); (5) microbialcontrol (biopesticides) (fungi, viruses, bacteria, nema-todes); (6) botanical pesticides and (7) chemical control(synthetic organic pesticides) [163, 164].Mechanical methods refer to the reduction or

suppression of insect populations by means of manualdevices. Some mechanical methods are hand picking,clipping, pruning and crushing to destroy insects androguing of disease affected seedlings. Although, mechanicalmethods are labour intensive they may be economical iflabour is abundant and not expensive. Mechanical practicesat the vegetative stage are the collection and destruction ofgirdle beetle infested plant parts and egg masses and theroguing of Seclerotium affected seedlings and yellow mosaicvirus affected soyabean plants (Table 9).Cultural control practices include all of the crop

production and management techniques that are utilized byfarmers to maximize their crop productivity and/or farm

income [163]. Cultural measures involve the manipulationof the agroecosystem to make it unfavourable for insectpests and more suitable for crop growth and naturalenemies of the pests. Cultural practices have potential ascomponents of IPM for farmers in the tropics becausethey are simple, effective, convenient, environmentallysafe, socially acceptable and economically feasible and donot require any limitation posed by pesticides to theenvironment, human health and development of pestresistance [165].Numerous cultural control practices are utilized in

managing soyabean pests, diseases and weeds (Table 9).Practices used in the stage between soyabean crops are croprotations, keeping soils covered with living vegetation,adding organic matter in the form of farmyard manure(FYM), vermicompost and decomposed crop residue,reduced tillage intensity and removal of infected stubblesfollowed by deep summer ploughing. Pre-sowing culturalpractices include the application of biofertilizers and soilnutrients such as NPK and S and selection of clean, diseaseand weed free seeds of high yielding insect pest and diseaseresistant/tolerant varieties. Cultural practices applied at thetime of sowing include sowing a trap crop, sowing time, seedrate and plant spacing. At the vegetative stage of soyabean,maintaining a weed-free crop for 30–45 days by handweeding, is an effective cultural control of weeds. Atharvest time, the crop should be harvested when 85% ofthe pods have turned brown for a shattering variety and80% for a non-shattering variety. Late harvesting, underhumid conditions, may result in the development ofPhomopsis, a fungal pathogen that results in reduced seedgermination.Host plant resistance as first described by Painter

[166] is ‘the relative amount of heritable qualities thatinfluence the ultimate degree of damage done by an insect’.In practical agriculture, resistance represents the ability of acertain variety to produce a larger crop of good quality thando ordinary varieties at the same level of insect population.This definition originally referred to insects, but has sincebeen broadened to include plant resistance to diseases.Globally, numerous soyabean varieties have been bred

for resistances/tolerance to soyabean insects and diseases.Based on previous knowledge of the most important pests,diseases and nematodes, in a given location, seeds ofresistant varieties can be selected in the pre-sowing phase.Table 9 provides a list of conventionally bred soyabeanvarieties with resistance/tolerance to four important insectpests and 12 important fungal, bacterial and viral diseases inIndia.GM soyabeans were first introduced in 1996 [167],

principally to make soyabean crops resistant to herbicides.Although resisted in some regions, notably Europe, GMsoyabeans are now grown in many parts of the world. Muchof the soyabean grown in Latin America and the USA(>90%) is GM to tolerate glyphosate herbicide. This meansthat soyabeans can be sprayed several times with thisherbicide during the growing season and all other plants,

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Table 9. Soyabean pest management package (modified from [90, 163])

Crop stage Management tactic Purpose

Between cropsCultural controlCrop rotations with cereal crops Break the continuity of soil-borne

pests as well as attract beneficialinsects and predatory birds

Add organic matter in the form of FYM, vermicompost,decomposed crop residue

To enhance below ground biodiversity

Reduce tillage intensity Conserve hibernating naturalenemies

The removal or destruction of stubble and crop residuesby burning, flooding or ploughing after the crop hasbeen harvested

Removes disease- andinsect-infected plants and exposessoil-borne pathogens, nematodesand insect-pests, and rhizomes andbulbs of perennial weeds

Pre-sowingField preparation Cultural control

Pre-sowing tillage Reduces the potential for carryover ofpest populations from one season toanother by exposing larvae todesiccation and predation

Apply balanced dose of biofertilizers and nutrients atrecommended rates as per the soil test

To promote good plant growth andcompete with weeds

Biological controlApply Trichoderma/P. fluorescens as a soil application For the management of seed,

seedling and seed-borne foliardiseases

Apply mycorrhiza and PGPR Promote plant growth and antagonismto soil-borne pathogens

Host plant resistanceSeed selection Selection of high yielding insect pest and disease resistant/

tolerant varieties mentioned below:Insect and disease control

Insect pest Resistant/tolerant varietiesStem fly JS 335, PK 262, NRC 12,

NRC 37, MACS 124 andMAUS 2, MAUS 47

Tobacco caterpillar JS 81-21, PS 564 and PK 472Green semilooper NRC 7, NRC 37, PUSA 16,

PUSA 20, PUSA 24, JS 93-05,JS 97-52, MAUS 47 andJS 80-21

Girdle beetle JS 71-05, NRC 7, JS 97-52,MAUS 32 and Indira Soya 9

Disease Resistant/tolerant varietiesRust PK 1024, PK 1029, JS 80-21,

Indira soyabean 9 and MAUS61-2

Sclerotium blight NRC 37Charcoal rot NRC 2, NRC 37, JS 71 05,

LSb 1, MACS 13 and JS 97-52Rhizoctonia aerial blight PK 472, PK 1042, PK 564 and

SL 295Anthracnose and pod blight Bragg, Himso 1563, PK 472,

JS 80-21, Pusa 37, VLS 21 andNRC 12

Bacterial pustule PK 1029, PK 1042, JS 71-05,JS 90-41, Bragg, Himso 1563,Indira soya 9, KHSb 2, MAUS32, NRC 7, NRC 37 and VLS 2

Yellow mosaic virus PK 416, PK 472, PS 564, PK1024, PK 1029, PK 1042, Pusa37, SL 295, SL 525, SL 688 andJS 97 52

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Table 9. (Continued)

Crop stage Management tactic Purpose

Soybean mosaic virus JS 71–05, KHSb 2, LSb 1, MACS58, MACS 124, Punjab 1 andVLS 2

Myrothecium leaf spot JS 71-05, JS 335, MACS 13,MACS 124, MAUS 47 andNRC 7

Purple seed stain JS 80-21 and BraggFrog eye leaf spot Bragg, JS 80-21, KHSb 2 and

VLS 21Alternaria leaf spot KHSb 2, NRC 2, PK 327, PK

1042, Himso 1563, JS 80-21,Pusa 37 and VLS 21

Cultural controlSeed cleaning Clean seeds to be sure they are free from disease infestation,

and weed seedsSeed germination Test seeds for germination before planting. The germination rate

should be 85% or moreTo avoid transferring diseases andweeds to the newly planted crop

Biological+ chemical control+ cultural control A good crop stand competes withweeds

Seed treatment Apply Trichoderma viride at 5 g or thiram 37.5%+carboxin37.5% DS at 3 g/kg seed

For the management of seed,seedling and seed-borne foliardiseases

This should be followed by seed treatment with Bradyrhizobiumand phosphate solubilizing bacteria (PSB) at 5 + 5 g/kg seed

Bradyrhizobium fixes nitrogen andPSB increases P uptake by theplant, both causing vigorous plantgrowth, which results in tolerance toinsect attack and competition withweeds

SowingCultural control

Sowing a trap crop Use of castor and dhaincha (green manure) as a trap crop Control of tobacco caterpillar andgirdle beetle respectively

Early planting of border strips as a trap crop Attract and control stink bugs andbean leaf beetle

Sowing time Cultivation of soyabean in rainy season only and sowing shouldbe done timely when soil moisture is sufficient (8–12 cmdepth)

To ensure proper germination andplant growth to compete with weeds

Seed rate Optimum seed rate (65–75 kg/ha) should be used dependingupon seed size. After every 15 rows, a gap of one row shouldbe given

To provide proper plant growth andprovide moving space for spraying instanding crop

Inter-cropping soyabean either with an early maturing variety ofDevil’s dung (asafoetida) (Ferula assa-foetida) or maize orsorghum in the sequence of four rows of soyabean with tworows of intercrop

Repel pests and promotesbiodiversity which will help toincrease and conserve naturalbiocontrol fauna e.g. coccinellidbeetles, Chrysoperla etc. In girdlebeetle and semilooper endemicareas, intercropping with maize orsorghum should be avoided

Row spacing Select proper row spacing as locally recommended Affect oviposition behaviour oflepidopterous pests

Plant spacing Sow soyabean by hand, planter, or by drilling. Plant three to fourseeds/hole at a spacing of 75 cm between rows and 10 cmbetween stands

Obtain maximum high-quality yieldsand limit the population and damageof insect pests by modifying theenvironment and influencing theeffectiveness of natural enemies

Vegetative stageMechanical practicesCollection and destruction of girdle beetle infested plant parts,egg masses

Control insect pests

Roguing of Sclerotium affected seedlings and yellow mosaicaffected plants

To prevent soyabean diseases fromspreading

Biological controlErection of bird perches at 10–12/ha Increase bird predation of insect pests

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but the soyabeans, will be killed. Recently more and moreweeds have become resistant to this herbicide, and there-fore, new GM soyabean varieties have been developed withmultiple herbicide resistance. As of 2017, 0% of thesoyabeans grown in India are GM.Biological control as defined by Van Driesche and

Bellows (1996) [168] is ‘the use of parasitoids, predators,pathogens and antagonists or competitor populations tosuppress a pest population, making it less abundant and lessdamaging than it would otherwise be’. Insects, mites,weeds, plant diseases and vertebrates all may be targetsof biological control. Biological control may be the result ofpurposeful action by man or may result from the unassistedaction of natural forces. Biological control may beemployed either for suppression of crop pests or forrestoration of natural systems affected by non-native(invasive) pests.As practiced, biological control can be self-sustaining and

distinguishes itself from all other forms of pest control byacting in a density dependent manner [169]. In a strictecological sense, applied biological control can be con-sidered a strategy to restore functional biodiversity

in agroecosystems by adding, through classical andaugmentative biocontrol techniques, ‘missing’ entomopha-gous insects or by enhancing naturally occurring predatorsand parasitoids through conservation and habitat manage-ment [170].In the Indian soyabean pest management package

at Pre-sowing it is recommended that Trichoderma orPseudomonas fluorescens, mycorrhizae and plant growthpromoting rhizobacteria (PGPR) be applied to the soil attime of field preparation for the management of soil-bornediseases (Table 9). These fungal and bacterial antagonistsare used to promote plant growth and provide the controlof plant diseases.Trichoderma is the most widely used biocontrol agent

[171]. Among the various isolates of Trichoderma, T. viride,T. asperellum, T. harzianum, T. virens and T. hamatum areused for the management of various diseases of crop plantsincluding the Fusarium, Phytophthora and Sclerotia genera.Trichoderma has many advantages including (a) highlycompetitive saprophytic ability, (b) enhances plantgrowth, (c) produces secondary metabolites/antibiotics ofvolatile and non-volatile nature, (d) provides a broad

Table 9. (Continued)

Crop stage Management tactic Purpose

Conserve spiders, coccinellid beetles, tachinid fly, prayingmantids, dragon fly, damsel fly, Chrysoperla and meadowgrass hoppers through biopesticides or minimum use of broadspectrum pesticides

To exploit maximum potential ofbio-control fauna

Release T. remus at 50 000/ha To control S. litura via eggparasitization

Microbial controlSpray B. thuringiensis var. kurstaki, serotype H-39, 3b, strainZ-52 at 0.75–1.0 kg/ha

For management of the semiloopercomplex (C. acuta, Gessoniagemma, D. orichalcea) and otherdefoliators

Botanical pesticidesSpray of NSKE at 5% For control of early stage larvae and

sucking pestsChemical controlApplication of pesticides should only be resorted if alternativepractices are not effective and pest population crosses theeconomic threshold

Management of insect pests andsoyabean diseases

Cultural controlMaintain optimum and healthy crop stand For the soyabeans to compete with

weedsThe crop should be maintained weed free initially for 30–45days by resorting two hand weedings

To prevent weed completion withsoyabeans

Reproductive stageFlowering Chemical control

Apply triazophos 40% EC at 625 ml/ha or chlorantraniliprole18.5% SC at 150 ml/ha

To control tobacco caterpillars, stemfly and girdle beetle

Pod development Poison baiting with 2% zinc phosphide at podding and greenseed stage preceded by 1 day pre-baiting or application ofbromadiolone 0.005%

Rodent control

HarvestTime Cultural control

Harvest when 85% of the pods have turned brown for ashattering variety and 80% for a non-shattering variety

To avoid development of seed-bornediseases e.g. Phomopsis whichreduce seed germination

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spectrum of action against various pathogens, (e) providesexcellent and reliable control, (e) is environmentallysafe and (f) is easy to multiply, even at the farm level[171, 172].Mycorrhizal fungi form a mutualistic relationship with the

roots of most plant species. In such a relationship, both theplants themselves and those parts of the roots that host thefungi are said to be mycorrhizal. Mycorrhizal plants areoften more resistant to diseases, such as those caused bymicrobial soil-borne pathogens.Bacteria that colonize plant roots and promote plant

growth are referred to as PGPR. PGPR are highly diverse.Their effects can occur via local antagonism to soil-bornepathogens or by induction of systemic resistance againstpathogens throughout the entire plant [173].Three biological control activities are listed at the

Vegetative stage (Table 9). (1) Erection of bird perches inthe field increases the number of birds which are predatorsof soyabean insect pests. (2) To exploit the maximumpotential of biocontrol fauna the conservation of naturalenemies (spiders etc.) of pest insects through the appli-cation use of biopesticides or the minimum use of broadspectrum of pesticides is recommended. (3) The release ofthe egg parasitoid, Telenomus remus is recommended tocontrol the armyworm, Spodoptera litura.Microbial control refers to the exploitation of disease

causing organisms to reduce the population of insect pestsbelow damaging levels. Microbial agents, also referred to asbiopesticides, that provide pest control include the viruses,bacteria, fungi and nematodes. Sprays of the bacterium,Bacillus thuringiensis var. kurstaki, are recommended for themanagement of the semi-looper and other defoliators atthe Vegetative stage in India (Table 9). Because biopesticidesare specific to the target pests, their natural enemies arenot affected. Some other biopesticides include the nuclearpolyhedrosis virus (NPV), the fungi Metarhizium anisopliaeand Metarhizium (Nomuraea) rileyi and entomopathogenicnematodes belonging to the families Heterorhabditidae andSteinernematidae.Botanical pesticides are agricultural pest management

agents whose active ingredients is are plant-producedchemicals. One of the most widely used botanical pesticidesis produced by the neem tree, Azadirachta indica, and iscommonly referred to as ‘neem’. Spray application of NeemSeed Kernel Extract (NSKE) is recommended in India forthe management of early stage insect pest larvae andsucking pests (Table 9).The neem tree is indigenous to India from where it has

spread to many Asian and African countries. For centuries,the tree has been held in esteem by Indian folk because ofits medicinal and insecticidal value. All parts of the neemtree possess insecticidal activity but seed kernel is the mostactive. Effects on insect pests have been reported to berepellency, antifeeding, growth inhibition, developmentdefects and even mortality [163].Neem products are safe to spiders, adults of numerous

beneficial insect species and eggs of many predators such

as coccinellids. Nymphal/larval instars are more orless susceptible, especially under laboratory conditions.As a rule, no or only slight side effects, are observedunder semi-field or field conditions. Due to their relativeselectivity (‘stage selectivity’), neem products can berecommended for many IPM programmes as it isunlikely that they will cause severe disturbances inecosystems [174].Chemical control (synthetic organic pesticides),

because of their environmental hazards, are only rec-ommended as a last resort, when other control measures inan IPM programme are not effective. In the soyabeanpackage of practices, pesticides are recommended at theVegetative stage for the control of insect pests and diseases(Table 9). In the reproductive stage, at time of flowering,triazophos (organophosphate) or chlorantraniliprole(anthracitic diamine, a reduced risk insecticide) arerecommended for control of stem fly, tobacco caterpillar,green semilooper and the girdle beetle.

Soyabean pest management under a changingclimate

In recent decades, climate change and the resultant globalwarming has become an issue of serious concern world-wide for existence of life on the earth [175, 176]. Over thepast 100 years, the global temperature has increased by0.8 °C and is expected to reach 1.1–5.4 °C by the end ofnext century. On the other hand, aberrant weather eventslike changes in rainfall patterns, frequent droughts andfloods, increased intensity and frequency of heat and coldwaves and outbreaks of insect-pests and diseases pro-foundly affect many biological systems and ultimately humanbeings [176].Extreme weather events, which occur in every agricul-

tural region of the world, cause severe crop damage. Thepersistent drought in the African Sahel has had the greatesthuman impact. In the USA, economic damage from singleevents can exceed $1 billion. The most severe, recentweather-related events were the drought of 1988 and theflood of 1993 [177].Despite remarkable improvements in technology and

crop yield potential, crop production remains highlydependent on climate because solar radiation, temperatureand precipitation are the main drivers of crop growth [177].Climate change, a long-term shift in the statistics ofweather, has a significant impact on agricultural pests. Thelast decade of the twentieth century and the beginning ofthe twenty-first century have been the warmest period inthe entire global temperature record [178]. The fourthassessment Report of the Intergovernmental Panel onClimate Change concluded that most of the observedincrease in the average global temperature since themid-twentieth century is very likely due to the observedincreases in the anthropogenic greenhouse gas concen-trations. It is now recognized that climate change will affect

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plant pests and diseases together with other components ofchange, i.e. anthropogenic processes such air, water andsoil pollution, long distance introduction of exotic speciesand urbanization [179]. Climate changes affect plants innatural and agricultural systems throughout the world[180]. Climate change directly impacts crops as well as theirinteractions with microbials [181].Climate has a significant effect on agricultural pests and

determines the extent of economic losses caused byinsects, pathogens and weeds. Globally, in 1995, annualsoyabean production was valued at US$24.2 billion.Estimated losses caused by pathogens, insects and weedswere $3.2, $3.7 and $4.7 billion respectively as reported[182]. Climate change is expected to significantly increasethose losses in many regions of the world.It has been reported that global climate warming may

lead to altitude-wise expansion of the geographic range ofinsect pests [183], increase in abundance tropical insectspecies [184] decrease in the relative proportion of thetemperature sensitive insect population [185], increasedincidence of insect-transmitted plant diseases throughrange expansion and rapid multiplication of insect vectors[186]. Therefore, with a changing climate it is expected thatfarmers growing crops will face new and intense pestproblems as global warming intensifies in years to come[187, 188].The spatial and temporal distribution and proliferation of

insects, weeds and pathogens is determined to a largeextent, by climate, because temperature, light and water aremajor factors controlling their growth and development.The geographical ranges of several important insects, plantpathogens and weeds in the USA have recently expanded,including the SCN (H. glycines) and soyabean sudden deathsyndrome (Fusarium solani f. sp. glycines) [181, 189, 190].For example, the SCN range expanded from the southernUS states in 1979 to the northernmost states borderingCanada in 1988. The soyabean sudden death syndromeexpanded from small, isolated areas in eastern Arkansas,and near the East Coast of North Carolina, to coveringmost of the eastern states [177].The major drivers of climate change are (1) increased

temperatures, (2) elevated CO2 levels, (3) precipitationchanges and (4) hurricanes, typhoons and wind currents.We will now discuss these four drivers.

Increased temperatures

The warming trend and changes in extremes can beexpected to affect the regional incidence of weeds,insects and crop pathogens. A change in the patterns ofprecipitation for crop–pest interactions may be even moreimportant than a change in the annual total rainfall [177].The water regime of pests is vulnerable to a rise in the dailyrate of and seasonal pattern of evapotranspiration resultingfrom warmer temperatures, drier air or windier conditions.Projected temperature increases can be expected to induce

earlier and faster development of crops, and causeincreased pest damage at the sensitive earlier stages ofcrop development [177].Warm winters increase the overwintering populations

of all pests and insect vectors of plant diseases [181] pests.For example, warm winters increase the population ofaphids (soybean aphid, A. glycines and other aphid species)that transmit soybean mosaic virus and increase the popu-lation and number of generations per year of the soybeandefoliator, the Mexican bean beetle, Epilachna varivestis,in the USA [177].Insects are particularly sensitive to temperature because

they are stenotherms (cold blooded). In general, insectsrespond to higher temperatures with increased develop-ment rates and with less time between generations. It hasbeen estimated that with a 2 °C temperature increase,insects might experience one to five additional life cyclesper season [191]. Therefore, global warming is expected tobenefit many insect species, especially in temperate regions,where crop losses will increase.Insect metabolism increases with temperature to a

certain point. When metabolism increases insects have toeat more [192]. If the temperature is too cold or too hot,the insect population will grow more slowly. This is thereason why crop losses will be greatest in temperateregions, but less severe in the tropics. Temperate regionsare not at the optimal temperature now, so if temperatureincreases there, insect populations will grow faster [192].Therefore, soyabeans grown in temperate zones such asChina, Japan and the USA will likely see increased insectdamage with increased global warming, whereas soyabeansgrown in the tropics, e.g. Africa and South America, will beless affected by global warming-induced insect damage.In insect species, limited by low temperatures at higher

latitudes, increasing temperatures reduce winterkill andresult in a greater ability to overwinter, therefore extendingthe insect species’ geographical range [183]. In Japan,warmer climates led to the northwards migration of thegreen stinkbug, N. viridula, a major agricultural pestdamaging the fruiting structures of soyabean, rice, cottonand other crops [193].As the globe warms, farmers will face more drought,

flooding and crop-damaging heat. In addition, highertemperatures will produce more voracious defoliatinginsects e.g. grasshoppers, caterpillars and other crop-devouring pests, with potentially catastrophic conse-quences for the world’s food supply. Scientists becamekeenly aware of the insect threat 10 years ago. That’s whenCurtis Deutsch et al. [194] published a study showing thatas temperatures rise, nearly all insects will multiply andincrease their metabolic rates.To determine what kind of damage this increased insect

appetite might have on the global food system, Deutsch andhis team built a computer program that combinedphysiological data on hundreds of insect species withclimate models. When the planet warmed by an averageof 2 °C, as models predict will happen by 2100, if not

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sooner, wheat crops shrunk by 46%, rice by 19% and maize(or corn) by 31%. Temperate, productive regions like theUnited States’ ‘corn belt’, wheat fields in France, and ricepaddies in China were especially hard hit, the team reportsin Science [195].Increased temperatures, humidity and precipitation

result in the spread of plant diseases as wet vegetationpromotes the germination of spores and the proliferation offungi and [188]. Under the warmer-but-drier conditions,projected for North America, crop losses due to plantdiseases are expected to decline up to 30%. However,under wetter conditions projected for Africa, losses todiseases are expected to increase by more than 100% forcertain crops.Temperature is the most important factor influencing

the biology of nematodes. Nematode developmental rateis directly influenced by temperature with slowerdevelopment at cooler and faster growth at warmer soiltemperatures. Therefore, an increase in atmospherictemperature, due to global warming, is expected to resultin more generations per season and an expansion of theirgeographical range [188].

Elevated CO2 levels

CO2 concentration in the atmosphere has increaseddrastically from 280 to 370 ppm and is likely to bedoubled by 2100 [176]. This change is attributed mainlyto the overexploitation and misuse of natural resources forvarious anthropogenic developmental activities such asincreased urbanization, deforestation and industrialization.Global climate models have projected the effects of

increasing atmospheric concentrations of greenhousegases. Simulations predict mean global warming ofbetween 1.5 and 5.8 °C (2.7 and 10.4 °F) by the end ofthe century. Because a warmer atmosphere can hold morewater vapour a mean global increase in global precipitationof 5–15% is predicted. Also, a warming trend can beexpected to affect the biophysical processes of photosyn-thesis and respiration, the regional infestations of weeds,insects and plant diseases and the thermal and hydrologicalregimes governing our agricultural systems [177].Increased CO2 levels can impact both the host plant and

the pathogen and insect herbivore in a multiple of ways[178]. New pathogen races and insect biotypes may evolverapidly under elevated temperature and CO2, as evolution-ary forces act on massive pest and pathogen populationsunder a favourable microclimate within an enlarged plantcanopy [196]. Higher growth rates of leaves and stemsobserved for plants grown under high CO2 concentrationsresult in denser canopies with higher humidity that favourspathogens. Denser canopies, which result in a greaterbiomass production and favourable microclimates, becomemore conducive for foliar pathogen development [188].Pathogen growth can be directly affected by higher CO2

concentrations resulting in increased fungal spore

production. A high concentration of carbohydrates in thehost tissue, due to elevated CO2 levels, promotes thedevelopment of biotrophic fungi such as rust [197]. Ingeneral, increased plant density will tend to increase leafsurface wetness duration and regulate temperatures, there-fore making infection by foliar pathogens more likely [198].Elevated CO2 levels can increase the extent of damage byleaf feeding insects, on soyabeans. During the early seasonsoyabeans grown in elevated CO2 atmosphere had 57%more damage from insects (including the Japanese beanbeetle, Popillia japonica; and the Mexican bean beetle,E. varivestis) than soyabeans grown in an ambient atmos-phere. The increased feeding under elevated CO2 levelsrequired that an insecticide be applied to be able tocomplete the experiment. The researchers surmised thatmeasured increases in the levels of simple sugars in thesoyabean leaves may have stimulated the additional insectfeeding [199]. Increased atmospheric CO2 is expected toalter the nutritional composition of crops, thereby affectingthe severity insect attack.Elevated levels of CO2, equivalent to those projected to

occur under global climate change scenarios, increase thesusceptibility of soyabean foliage to herbivores by down-regulating the expression of genes related to the defensehormones, jasmonic acid and ethylene; these in turndecrease the gene expression and activity of cysteineproteinase inhibitors (CystPIs), the principal antiherbivoredefenses in foliage [200].To determine the effects of elevated CO2 on the

preference of the Japanese beetle (P. japonica) for soyabeanleaves of different ages within the plant, a study wasconducted at the University of Illinois [200]. When given achoice, the Japanese beetle inflicted greater levels ofdamage on older leaves than on younger leaves, and therewas a trend for a greater preference for young leaves grownunder elevated CO2, compared with those grown underambient CO2. The more damaged older leaves and thosegrown under elevated CO2 had reduced CystPI activity.CystPIs are potent defenses against the Japanese beetle,and the effectiveness of this defense is modulated bygrowth under elevated CO2, as well as leaf position[199, 201, 202].Enhanced CO2 levels increase the biological control

activity of generalist predators [203]. The herbivorouscotton bollworm (H. armigera) larvae feeding on elevatedCO2-grown pea (Pisum sativum) at 700 ppm were signifi-cantly smaller than those grown on ambient CO2-grownplants. The omnivorous, spined predatory shield bug(Oechalia schellenbergii) performed best when fed onbollworm larvae from the elevated-CO2 treatment, appar-ently because the H. armigera prey was smaller and thuseasier for the predator to overcome. Taken together,results indicate that elevated CO2 may benefit generalistpredators through increased prey vulnerability, whichwould put pest species under higher risk of predation [203].Global warming means more pests, including weeds

[204]. Plants are divided into C3 and C4 types, according to

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how they utilize CO2, in photosynthesis. Wheat, rice andsoyabeans are C3 plants. C3 plants respond to increasedCO2 concentration with increased growth. Maize, sorghumand sugarcane are C4 plants and are less responsive to anincrease in CO2. Weeds also follow this division [204].Therefore, increased CO2 levels encourage the growth ofC3 weeds and increase the water use efficiency of both C3and C4 weeds. Increased temperatures promote thegrowth of C4 weeds [205]. For this reason, subtropicalC4 weeds in the USA are likely to spread northwards aswinter temperatures in northern climes become warmerwith global warming. Also, it is predicted that, perennialweeds in soyabean and other crops may be more difficult tocontrol, since increased photosynthesis, due to increasedCO2, may lead to greater storage of food supplies.

Precipitation changes

Precipitation – whether optimal, excessive or insufficient –is a key variable that affects crop–pest interactions [188].Some insects are sensitive to precipitation and are killed orremoved from crops by heavy rains. Drought stress hasbeen reported to result in increased pest outbreaks. It hasbeen shown that drought stress can affect the physiology ofplant host species, leading to changes in the insects that feedon them [206]. Abnormally cool, wet conditions can alsocause severe insect infestations.Increased precipitation, due to heavy rains, benefits

epidemics and prevalence of leaf fungal pathogens [188].The heavy rains in 1993, which caused flooding anddamaged crops in over 11 million acres, caused fungalepidemics in maize, soyabean, alfalfa and wheat in the USGreat Plains. Heavy rains in north central USA in 1993,caused outbreaks of soyabean sudden death syndrome,caused by the soil-borne root pathogen, F. virguliforme,formerly known as F. solani f. sp. glycines [188].Fungal pathogens of insects are favoured by high humidity

and their incidence is increased by climate changes thatlengthen periods of high humidity and reduced by thosethat result in drier conditions [188]. Chen and McCarl[207] investigated the relationship between precipitationand pesticide costs in the USA and concluded that increasesin rainfall lead to increases in average pesticide costs forcotton, maize, soyabean and wheat.The severe drought of 1988 in the US Midwest,

accompanied by higher than normal temperatures, beganearly in the spring and continued throughout most of thesummer [208]. Crop yields dropped by approximately 37%and required a $3 billion government bailout for farmers.The drought impacted crop pests, with outbreaks of thetwo-spotted spider mite (Tetranychus urticae) damagingsoyabeans throughout the entire Midwest region. Mitedamage occurred during the critical flowering, pod devel-opment and pod filling growth stages. To control the mite,insecticide was applied to about 3.2 million hectares.

Losses to Ohio farmers alone were estimated at$15–20 million [209].Water stress, due to drought, decreases plant vigour and

alters the C/N ratio which in turn lowers the level of plantresistance to the feeding of nematodes and insects.Outbreaks of the SCN (H. glycines) correlated withdrought conditions in the north central USA in 1990 [177].

Hurricanes, typhoons and wind currents

Hurricanes and wind currents provide large-scale trans-portation for disease agents (e.g. fungal spores) and insectsfrom overwintering areas [181]. Asian soyabean rust(P. pachyrhizi) is an exceptionally aggressive pathogen thathas rapidly spread globally since about 2000, moving fromAsia through Africa and on to South America [210]. InSeptember 2004, hurricane Ivan struck the US Gulf Coastintroducing P. pachyrhizi into Louisiana, and by December2004 there were 20 new detections in eight states, outliningthe periphery of the hurricane impact zone [211].

Rise and Demise of Soyabean Pest Management:The Brazilian Example

Introduction

The history and evolution of the soyabean IPM programmein Brazil, like elsewhere in the world, is linked to the abusiveuse of pesticides and the subsequent results [212, 213]. Theover-use of pesticides led to government policies tomitigate the side effects of pesticides, and a majorcomponent of this change was the implementation of IPMprogrammes [214].The chronological development of the soyabean pest

management programme in Brazil can be broken down intofour eras: (1) the beginning years – 1970s, (2) theBaculovirus era – 1980s, (3) the 1990s – egg parasitoidera and (4) soyabean insect management in the newmillennium. This section discusses the tremendous levelof adoption of soyabean pest management by Brazilianproducers (2 million hectares under soyabean pest manage-ment in the 1980s) [215] and the subsequent decrease inthe current area under soyabean pest management (almostnil) due to changes in agronomic practices [214].

The beginning years – 1970s

Soyabean pest management was perhaps the most success-ful pest management programme developed in Brazil [214]and most likely the largest, most prominent and successfulsoyabean pest management programme in the world.However, it was initially an insect management programmeand it was not until the later years that diseases and weeds

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were integrated into the programme resulting in an IPMprogramme.The commercial cultivation of soyabeans in Brazil began

expanding in the 1970s. The predominant method of pestcontrol was exclusively based on the use of insecticides andacaricides [216, 217]. During this period an average of fivepesticide applications (varying from three to ten) weremade per soyabean crop [218]. The insecticides applied,such as dieldrin, DDT, toxaphene and methyl parathionwere broad spectrum products and highly toxic to humansand the natural enemies [218].In 1972, the Brazilian government, in collaboration

with the University of Wisconsin/USAID, established theProjeto Nacional da Soja (National Soybean Project) withheadquarters at the Rio Grande do Sul State Departmentof Agriculture in Porto Alegre. In 1973, with theestablishment of EMBRAPA, the project became theEMBRAPA-Soja Program. In 1975, the program moved toLondrina and joined the Agronomic Institute ofParaná-IAPAR. There, the EMBRAPA-Soja program,EMATER-Parana, and some Brazilian and US universitiesbegan pioneering work on IPM in soyabean, primarily to thepromote the rational use of insecticides to growers. ThePorto Alegre project provided some of the basic infor-mation later used in the development of pest managementcomponents and provided opportunities for Brazilianstudents to conduct MS theses on soyabean pest manage-ment subjects. Of the numerous students who conductedresearch in the areas of entomology, nematology, plantpathology, weed science and plant breeding, many have hadlong careers at EMBRAPA, and have retired, and some arestill active in soyabean research. These scientists are theones that are responsible for the development of theBrazilian soyabean pest management programme.Due to the overuse of pesticides in Brazilian soyabean

production institutions such as EMATER-PR, theAgronomic Institute of Paraná-IAPAR, and some univer-sities began pioneering work on IPM in soyabean [34]. IPMwas based on the premise that cultivated plants can toleratecertain levels of injury without economically significantyield reductions; and insecticides should be used only as acomplementary method, since natural biological controlmust be responsible for keeping pests under control. Thus,in the 1970s, economic thresholds were established for themajor soyabean pests, the defoliating caterpillars and seedsucking stink bugs.Pilot projects were conducted with extension agents to

test the IPM technologies developed. Brazilian personnelwere trained on the use of selective insecticides for theprotection of natural enemies [34]. The first major impactwas a reduction in the amount of insecticide used tocontrol pests. The IPM concepts were then rapidly adoptedby the extension personnel who passed the message on tothe growers. After only 3–4 years of soyabean IPMadoption in Brazil, the application of pesticides in soyabeanwas reduced from an average of five applications to onlytwo applications per season [214]. The soyabean IPM

approach radically changed the common practice ofexpensive, preventative, calendar-based insecticide appli-cations to a more economically profitable and environmen-tally safe insect control strategy [214].

The Baculovirus era – 1980s

In the 1970s and 1980s, the major lepidopterous soyabeanpest in southern Brazil was the velvetbean caterpillar,A. gemmatalis [219, 220] which caused severe defoliationof soyabean plants [214]. The fungal entomopathogen,M. (Nomuraea) rileyi [221] is responsible, especially in rainyseasons, for maintaining A. gemmatalis populations undercontrol and when the infestation is timely, virtuallyeliminates the requirement of insecticide to control thesepests [39].Another naturally occurring biocontrol agent, a nuclear

polyhedrosis virus, Baculovirus anticarsia, was also found tobe effective in providing natural control [222, 223]. Thisvirus was referred to as AgNPV (A. gemmatalis nuclearpolyhedrosis virus). A pilot programme to develop the useof AgNPV was developed and implemented [224]. The pilotproject, initially tested in the states of Parana and RioGrande do Sul, rapidly spread to other states and reachednearly 1.6 million hectares, representing about 10% of thetotal area cultivated with soyabean in Brazil [178]. TheAgNPV initially applied consisted of a homemade solutionmade from field collected diseased A. gemmatalis larvae(50 larvae equivalents/ha). Later, a wettable powderformulation was developed and widely used [187]. In theearly 2000s, an area of approximately 2.0 million hectareswas treated with baculovirus, representing a savings ofabout 2 million litres of insecticides. The addition of theAgNPV component dramatically increased the effectivenessand success of the Brazilian soyabean IPM programme. Dueto the success of the programme in Brazil, it was adoptedby other Latin American countries [225].

The 1990s – egg parasitoid era

In the 1990s, a new control tactic, the biological control ofsoyabean stink bugs with egg parasitoids was added to theBrazilian soyabean IPM programme. The objective was toachieve a more stable control by augmenting the number ofthese beneficial agents and by conserving field populationsof stink bug parasitoids [226].Thirty-two species of stink bugs (Hemiptera:

Pentatomidae) have been reported in soyabean in Brazil[50] and several are considered as important soyabeanpests. They feed on the developing grains which results infoliar retention [227], reduced grain quality [228] due tothe transmission of yeast spot disease, N. coryli [229], andsevere yield reduction [230–232]. There are more than20 species of parasitoids providing natural biologicalcontrol of stink bugs in Brazilian soyabean fields [233].

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The most important species are Trissolcus basalis, thatpreferentially attacks N. viridula eggs, and Telenomus podisithat prefers eggs of E. heros and P. guildinii [214]. However,these parasitoids tend to occur in high populations, whenthe stinkbugs have already reached economic thresholdlevels. For this reason, a programme for laboratoryproduction and inoculative release was developed at theEmbrapa Soyabean project at Londrina, PR [234].After 4 years of field tests, a pilot programme was

developed in collaboration with the Paraná state extensionservice, using T. basalis [235]. Cards with T. basalisparasitized stinkbug eggs were placed at the edge ofsoyabean fields (where stinkbug infestations generallybegin), at the rate of 5000 egg parasitoids/ha, at the finalflowering stage [236].To increase the effectiveness of egg parasitoids for stink

bug control, growers were recommended to use AgNPV tocontrol the velvetbean caterpillar. To control otherlepidopterous defoliators, and to avoid killing egg para-sitoids that colonize the fields early in the season, growerswere recommended to use microbial and/or selectiveinsecticides such as those based on Bacillus thuringiensis orinsect growth regulators (e.g. diflubenzuron).Following the successful results of the pilot project, the

stinkbug parasitoid technology was implemented at thefarm level in the 1993/94 season. In 1994/95 a modifiedprogramme was deployed in the micro river basins ofParaná state consisting of 18 020 ha and 343 soyabeanproducers. Before implementation of the project, stinkbugparasitism was low [50]. After implementation of theIPM programme 90% of N. viridula, 65% of P. guildinii and78% of E. heros eggs were killed by egg parasitoids [237].The mean number of insecticide applications percropping year in the river basin fell from 2.8 (1993/94season) to 1.23 four seasons later. Area under biocontrolof the velvetbean caterpillar with AgNPV increased57%, from 205 ha in the 1993/94 season to 2730 ha in1998 [238].It is important to note that during the 1990s, several

other components were added to the soyabean IPMprogramme in Brazil. This included economic thresholdsto control the coleopterous stem borer, Sternechussubsignatus [39] and the application of insecticides, onlyon the border rows, or at a reduced dosage, mixed withsodium chloride to control stink bugs [239]. After theadoption of soyabean IPM in the 1980s, the use ofinsecticides in Brazil was reduced to about two applicationsper season [240].

Soyabean Insect Management in theNew Millennium

Over the last 40 years, soyabean yield in Brazil has doubled,increasing from an average of <1500 kg/ha in the 1970s tomore than 3000 kg/ha in 2015 [240]. The yield increase,along with higher soyabean prices, the lower cost of many

insecticides, the change in agronomic practices and thefailure to use economic thresholds and pest monitoring[241], have led to the abandonment of soyabean IPM inBrazil. Consequently, insecticide applications again reachedan average of four to six and even more sprays per cropcycle, impairing the effectiveness of all existing biologicalcontrol agents for soyabeans [242].What specifically were the factors that led to the demise

of soyabean IPM in Brazil? Why wasn’t the IPM programmesustainable? In the 1970s, at the beginning of the soyabeanIPM implementation in Brazil, the conventional cultivationsystem was practiced on 100% of the soyabean area. Thiscultivation system included several machinery operations totill and level the soil. This system was eventually abandoned,mainly due to the severe erosion, loss of soil nutrients, anddue to economic reasons. Then, the no-tillage cultivation, anew system was proposed and implemented. Under thissystem the soil is left undisturbed and covered with cropresidues from the previous wheat crop. The change wasdramatic: from <5000 ha under no-tillage at the beginningof the 1970s to 32 million ha in 2013. This change, althoughimportant from an ecological and economical point of view,severely impacted the IPM system practiced by soyabeangrowers [214].Because of no-till cultivation, many soil-inhabiting pests

increased in importance and were damaging soyabeanplants at the beginning of the cultivation season. Tocontrol these pests, insecticide applications were requiredand these applications disrupted the needed balance ofpests versus natural enemies. As a result, polyphagous peststhat live on or in the ground such as the root suckingburrower, Scaptocoris castanea [243], tropical brown stinkbug, E. heros, [244], green belly stink bugs, Dichelopsfurcatus and D. melacanthus and several species of root-feeding beetles [245] were favoured and their populationssignificantly increased. This was essentially the beginning ofthe end of soyabean IPM in Brazil.The current system of multiple cropping has also

contributed to increasing pest populations and wasanother dagger in the heart of an already weakenedsoyabean IPM programme. Multiple cropping with soyabeanand/or maize double cropping without a break, provides afood resource for pests throughout the year. These pestsneeded to be controlled, if high yields were to be achieved,and the major control agent was pesticides that destroyedthe natural enemy population.The next dagger, in the heart of the IPM programme, was

the unsustainability of the use of the biological controlagent, AgNPV, to control the velvetbean caterpillar.Because of the difficulty of producing AgNPV the demandwas much greater than the supply [15]. Lack of informationabout the use of AgNPV was the primary cause for theunsuccessful application of this biological control agent.First, the growers who were accustomed to the fast actionof insecticides did not appreciate the delayed mode ofaction of AgNPV. Second, most growers, many withextremely large fields, were unprepared for the careful

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monitoring of A. gemmatalis phenology necessary to ensureeffective application of AgNPV [225]. For these reasons, inregions where the extension programme was weak, the useof the virus was negligible [246].Another setback for soyabean IPM in Brazil was a

reduction in the costs of conventional insecticides whichwere toxic to natural enemies of soyabean pests, and theirsubsequent increased use. In addition, the mixture insecti-cides with herbicides to control weeds exacerbated theproblem. Moreover, because of the increased insecticideuse, secondary pests such as chewing caterpillars that feedon pods and leaves (Spodoptera spp. and soyabean looper,Pseudoplusia includens), and mites, thrips and whitefliesincreased in their abundance and gained the status of majorpests [214].Finally, the arrival and spread of the soyabean rust fungus,

P. pachyrhizi, had a significant impact on the soyabean IPMprogramme. Some of the most effective fungicides forcontrolling rust were harmful to the naturally occurringentomopathogenic fungi such as M. (Nomuraea) rileyi andothers [247]. This added even more pressure to the alreadyweak role that the natural enemies and insect pathogenswere already playing due to the change in cultural practices.The various factors mentioned above led to a completecollapse in the use of the classical and highly successfulsoyabean IPM programme in Brazil by the end of2010 [214].Recently, consideration of IPM has been revived with the

introduction of a new pest in the Americas. In Brazil,H. armigera was identified for the first time in February2013 [248]. Damage estimates reached US$0.8 billion inthe first crop season. The Brazilian government, through-out its institutions, established a task force to train most ofthe growers and consultants to identify and control the pestcorrectly.An encouraging factor is that the private industry is

providing strong support in the promotion of soyabean IPMin Brazil. For example, during the last season (2016/2017)the egg parasitoid, Trichogramma pretiosum, was released inmore than 2 million ha of soyabean in Brazil for thebiological control of H. armigera. In fact, the demand is sohigh that the companies producing the Trichogramma arenot able to meet the farmers’ requests. In addition, thiscrop season (2017/18), the company, BUG – Piracicaba, willsell the stink bug egg parasitoid T. podisi. Again, theproduction will not be able to meet the farmer demandbecause of the difficulty of production. Rearing is difficultbecause the egg host needs to be stored in liquid nitrogen(F. Goncalves, Personal Communication).Therefore, if on the one hand, H. armigera brought some

yield losses to Brazilian growers in its first years in thecountry, on the other hand, the presence of this pestbrought back the need to employ some old IPM conceptsthat had almost been forgotten by most growers. With thepresence of H. armigera in Brazil, growers are learning thatto address the insect problems and still maximize agricul-tural production.

With the development of transgenic soyabeans for insectand weed control, the presence of invasive pests such asH. armigera, the planting of early maturity varieties andindeterminate cultivars, and the availability of environmen-tally friendly biopesticides and egg parasitoids, agronomicpractices (e.g. crop rotation and the new conventionallybred pest resistant varieties), and reliable economicthresholds [241, 249, 250], there is an urgent need todesign modern, sustainable soyabean IPM programmes forBrazilian growers [214].This subject has been discussed in several forums [214].

There is a consensus, among Brazilian scientists, that thereis an urgent need that the government develop legislationthat promotes IPM as an official governmental policy and tostimulate governmental funding agencies to support IPM,not only for soyabeans, but also for all major commodities.It is envisaged that that private industries should collaboratewith publicly supported agencies, international agencies andNGOs, to support on a regional scale, IPM programmesthat yield long-term benefits, not only to growers, but alsoto the broader community [214].However, Brazilian IPM scientists have a monumental

barrier to overcome in implementing a return to IPM inBrazil. Governmental policies have significantly erodedwhat remained of IPM in Brazil. In 2013, the last yearfigures are available, Brazilian buyers purchased $10 billionworth, or 20% of the global pesticide market. Since 2008,Brazilian pesticide demand has risen 11% annually – morethan twice the global rate [251].The Brazilian farmers have become the world’s top

exporters of sugar, orange juice, coffee, beef, poultry andsoyabeans. This rapid growth has made Brazil an enticingmarket for pesticides, banned or phased out in richernations, because of health or environmental risks. Inaddition, they have earned a more dubious distinction: in2012, Brazil passed the United States as the largest buyer ofpesticides [251].This excessive, and misuse, of pesticides has led to many

cases of insecticide poisoning and contamination of thefood supply. One factor blocking safeguards, that are moreforceful, is Brazil’s increasingly powerful agricultural lobby.The industry’s influence, and tight budgets for regulators,limits Brazil’s ability to enforce pesticide regulations [251].Consider the time it takes Anvisa, the federal agency in

charge of evaluating pesticide health risks, to evaluate aproposal by a manufacturer to sell a pesticide in Brazil. Bylaw, the agency is supposed to analyse a new chemical in nomore than 120 days. However, Anvisa can take years tocomplete this process. With fewer than 50 scientists,compared with hundreds at comparable agencies in theUnited States or Europe, it has a backlog of more than 1000chemicals awaiting review [251]. This severely limits theintroduction of alternatives to pesticides, such as biologicalcontrol agents and microbial agents, that are environmen-tally acceptable, in IPM programmes.IPM programmes are greatly influenced by regulatory

mechanisms in place to manage the handling and use of

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pesticides. These regulatory activities include pesticideregistration, banning of unsafe pesticides, food safety, farmworker safety and prevention of pest resistance. Indeed,favourable governmental policies are the key to IPMadoption. If policies create barriers to IPM adoption, suchthat there is little economic incentive to adopt, there maybe little return to IPM research and extension [252]. TheBrazilian IPM scientists have their marching orders. Policiesand actions affecting IPM adoption in Brazil need to bemodernized in favour of consumers, growers andbiodiversity.

Acknowledgement

Preparation of this review was supported by the USAIDCooperative Agreement No. AID-OAA-L-15-00001awarded to Virginia Tech.

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